Charles Darwin University
Ice ages and butterflyfishes
Phylogenomics elucidates the ecological and evolutionary history of reef fishes in anendemism hotspotDiBattista Joseph D Alfaro Michael E Sorenson Laurie Choat John H Hobbs JeanPaul A Sinclair-Taylor Tane H Rocha Luiz A Chang Jonathan Luiz Osmar J CowmanPeter F Friedman Matt Berumen Michael LPublished inEcology and Evolution
DOI101002ece34566
Published 01112018
Document VersionPublishers PDF also known as Version of record
Link to publication
Citation for published version (APA)DiBattista J D Alfaro M E Sorenson L Choat J H Hobbs J P A Sinclair-Taylor T H Rocha L AChang J Luiz O J Cowman P F Friedman M amp Berumen M L (2018) Ice ages and butterflyfishesPhylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot Ecologyand Evolution 8(22) 10989-11008 httpsdoiorg101002ece34566
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Download date 23 Aug 2020
Ecology and Evolution 2018810989ndash11008 emsp|emsp10989wwwecolevolorg
Received12May2018emsp |emsp Revised19August2018emsp |emsp Accepted29August2018DOI 101002ece34566
O R I G I N A L R E S E A R C H
Ice ages and butterflyfishes Phylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot
Joseph D DiBattista123 emsp|emspMichael E Alfaro4emsp|emspLaurie Sorenson4emsp|emspJohn H Choat5emsp|emsp Jean‐Paul A Hobbs3emsp|emspTane H Sinclair‐Taylor1emsp|emspLuiz A Rocha6emsp|emspJonathan Chang4 emsp|emsp Osmar J Luiz7emsp|emspPeter F Cowman8emsp|emspMatt Friedman910emsp|emspMichael L Berumen1
1RedSeaResearchCenterDivisionofBiologicalandEnvironmentalScienceandEngineeringKingAbdullahUniversityofScienceandTechnologyThuwalSaudiArabia2AustralianMuseumResearchInstituteAustralianMuseumSydneyNewSouthWalesAustralia3SchoolofMolecularandLifeSciencesCurtinUniversityPerthWesternAustraliaAustralia4DepartmentofEcologyandEvolutionaryBiologyUniversityofCaliforniaLosAngelesLosAngelesCalifornia5CollegeofScienceandEngineeringJamesCookUniversityTownsvilleQueenslandAustralia6SectionofIchthyologyCaliforniaAcademyofSciencesSanFranciscoCalifornia7ResearchInstitutefortheEnvironmentandLivelihoodsCharlesDarwinUniversityDarwinNorthernTerritoryAustralia8ARCCentreofExcellenceforCoralReefStudiesJamesCookUniversityTownsvilleQueenslandAustralia9DepartmentofEarthSciencesUniversityofOxfordOxfordUK10MuseumofPaleontologyandDepartmentofEarthandEnvironmentalSciencesUniversityofMichiganAnnArborMichigan
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd
CorrespondenceJosephDDiBattistaAustralianMuseumResearchInstituteAustralianMuseumSydneyNSWAustraliaEmailjosephdibattistagmailcom
Funding informationKAUSTOfficeofCompetitiveResearchFundsGrantAwardNumberCRG-1-2012-BER-002AustralianResearchCouncilGrantAwardNumberDE170100516NationalGeographicSocietyGrantAwardNumber9024-11NationalScienceFoundationGrantAwardNumberDE170100516
AbstractFortropicalmarinespecieshotspotsofendemismoccurinperipheralareasfurthestfromthecenterofdiversitybuttheevolutionaryprocessesthatleadtotheiroriginremain elusiveWe test several hypotheses related to the evolutionof peripheralendemicsbysequencingultraconservedelement (UCE) locitoproduceagenome-scalephylogenyof47butterflyfishspecies(familyChaetodontidae)thatincludesallshallowwaterbutterflyfishfromthecoastalwatersoftheArabianPeninsula(ieRedSeatoArabianGulf)andtheircloserelativesBayesiantreebuildingmethodspro-ducedawell-resolvedphylogenythatelucidatedtheoriginsofbutterflyfishesinthishotspotsofendemismWeshowthatUCEsoftenusedtoresolvedeepevolutionaryrelationshipsrepresentanimportanttooltoassessthemechanismsunderlyingre-centlydivergedtaxaOuranalysesindicatethatuniqueenvironmentalconditionsinthecoastalwatersoftheArabianPeninsulaprobablycontributedtotheformationofendemicbutterflyfishesOlderendemicspeciesarealsoassociatedwithnarrowver-sus broad depth ranges suggesting that adaptation to deeper coral reefs in thisregionoccurredonlyrecently(lt175Ma)Eventhoughdeepreefenvironmentswere
10990emsp |emsp emspensp DIBATTISTA eT Al
1emsp |emspINTRODUC TION
Explaining the underlying factors responsible for the diversity ofspecies accumulated at hotspots of endemism remains a difficultprobleminthefieldofbiogeographyRecentresearchhasidentifiedtheimportanceofperipheralregionsfromtropicaloceansingener-atingandexportingbiologicaldiversitythusintermittentlyseedingadjacent seas (BowenRocha ToonenampKarl 2013DiBattista etal2013DiBattistaWilcoxCraigRochaampBowen2010Ebleetal2011Gaitheretal2011GaitherToonenRobertsonPlanesampBowen2010MalayampPaulay2010SkillingsBirdampToonen2010)howeverdirecttestsofthisassumptionarerareRenewedinterestin theRedSea toArabianGulf (orPersianGulf) regionprovidesanew opportunity to explore hypotheses associated with how en-demicsareformedinperipheralareasanditspotentialcontributiontothespeciesrichnessofmarinebiodiversityhotspotsTheRedSeaisasemi-enclosedbasinlocatedatthenorth-westerncorneroftheIndianOceanandharborsoneofthehighestlevelsofendemismformarineorganisms(129forfishes126forpolychaetes81forechinoderms 165 for ascidians and 58 for scleractinian cor-alsDiBattistaRobertsetal2016)Thelevelofendemismamongwell-characterizedgroupsintheRedSeasuchastheshorefishesexceedsthoseofallotherperipheralendemichotspotsidentifiedfortheIndianOcean(DiBattistaRobertsetal2016)AlthoughmanyoftheseRedSeaendemicsextendtheirdistribution intotheadja-centGulfofAdenandArabianSea(DiBattistaChoatetal2016DiBattistaRobertsetal2016Kemp1998)itisnotclearwhethertheyarepaleo-endemics(oldlineagesrestrictedduetorangecon-traction) neo-endemics (young lineages at the site of origin) orldquoecologicalrdquoendemics(oldoryounglineageswitharestrictedrangeduetospeciesecologyseeCowmanParraviciniKulbickiampFloeter2017)andwherewhenandhowthisdiversificationoccurred
TheRedSeahasauniquegeologicalandpaleoclimatichistorythatmayhaveplayedaroleinitshighlevelsofendemism(seeDiBattistaChoatetal2016forreview)InbrieftheRedSeabasinwasformedbyepisodesofseafloorspreading41ndash34Ma(GirdlerampStyles1974)followedby intermittentconnections to theMediterraneanSea inthe north (~14ndash5MaHubert-Ferrari et al 2003) and amore re-centconnectiontotheGulfofAdeninthesouththroughtheStraitofBabalMandab (~5Ma topresentBailey2010)TheStrait isanarrowchannel (29km)withashallowsill (137m)thatconstitutesthe only connection between the Red Sea and the Indian Ocean
(Bailey2010)Waterexchange is regulatedby IndianOceanmon-soonpatterns(RaitsosPradhanBrewinStenchikovampHoteit2013Smeed1997)butwashistoricallyminimalorabsentduringreducedsealevelscausedbyglacialperiodsofthePleistocene(Rohlingetal2009)includingthemostrecentglacialmaximum(20ndash15kaLudtampRocha2015Siddalletal2003)RestrictedwaterflowresultedinincreasedsalinitywithintheRedSea(BitonGildorampPeltier2008)leadingsometosuggestthattherewascompleteextirpationofRedSeafaunaduringtheseperiods(Klausewitz1989)TheldquoPleistoceneextirpationrdquohypothesiswhereinallRedSeafaunawereeliminatedduringthe lastglacialmaximum(~18ka)andsubsequentlyre-pop-ulated via more recent colonization events remains controversialand untested with modern comparative approaches (DiBattistaChoatetal2016)althoughsimilargeologicaleventsmayhaveoc-curredintheMediterraneanSea(Bianchietal2012)Thusdespitesomeagreementonthebroadstrokesof itsgeologichistory littleconsensushasemergedontheprocessesthatshapedtheArabianPeninsularsquospresentdaymarinebiodiversitytheirinfluenceonbiodi-versityinadjacentregionsandtheroleofhistoricalclosuresoftheStraitofBabalMandab
ButterflyfishesandbannerfishesbrightlycoloredreeffishesinthefamilyChaetodontidaeareapotentialmodelsystemforeluci-datingtheoriginsmaintenanceandevolutionaryhistoryofRedSeaendemicsandtheirinfluenceonspeciesrichnessinadjacentmarineregionsThefamily isdiverse (17species intheRedSeaandgt130species in the greater Indo-West Pacific Allen Steene amp Allen1998)andphylogeneticallywellresolvedcomparedtootherreeffishfamilies(Cowman2014)AhighproportionoftheChaetodontidaespecies found in the coastal waters of the Arabian Peninsula areendemic (32 DiBattista Roberts et al 2016) Although recentmolecularphylogeniesofchaetodontidshavehelpedtoclarifymanyaspectsoftheirevolutionaryhistory(Bellwoodetal2010Cowmanamp Bellwood 2011 2013 Fessler amp Westneat 2007 HodgeHerwerdenampBellwood2014HsuChenampShao2007)alackofsamplingofArabianPeninsulaspecieshasimpededourunderstand-ingofthediversificationinthisregion
Theevolutionofendemicspecieshasbeenlinkedtoecologicaltraits such as reductions indispersal ability and changes inbodysize(ietheislandrulereviewedbyLomolino2005WhittakerandFernaacutendez-Palacios2007)Forreeffishescertaintraitsassociatedwith dispersal ability are linked to geographic range size For ex-amplelargegregariousandnocturnalspeciestendtohavelarger
drasticallyreducedduringtheextremelowsealevelstandsofglacialagesshallowreefspersistedandassuchtherewasnoevidencesupportingmassextirpationoffaunainthisregion
K E Y W O R D S
biogeographicbarriersChaetodoncoralreefglaciationeventsPleistoceneultraconservedelements
emspensp emsp | emsp10991DIBATTISTA eT Al
rangesizesthansmallsolitaryandstrictlydiurnalspecies(Luizetal20132012)Moreoverdispersalabilitycanpotentiallyinfluencecladediversificationtosuccessfullycolonizeandestablishpopula-tionsinperipheralareastropicalfishspeciesmustbegooddispers-ers(HobbsJonesMundayConnollyampSrinivasan2012)Followingdiversification in peripheral areas newly formed lineages mayevolvetraitslessconducivetodispersalthusbecomingendemictotheareawhereitoriginatedasoftenoccursintheevolutionofinsu-larterrestrialendemics(WhittakerandFernaacutendez-Palacios2007)We thereforepredict thatbutterflyfishesendemic to theArabianPeninsularegionwillhavesmallerbodysizeshighersociabilityandreduceddispersalabilitycomparedtotheirwidespreadcongenersBroadly speaking endemic species tend to be ecological special-istsandthusadaptedtotheenvironmentalconditioninwhichtheyarose (McKinney 1997) We therefore additionally predict thattheseendemicswillhaveahigherlevelofecologicalspecializationthanwidespread species For reef fishes habitat specialization isoftendefinedbythedepthrangewheretheyoccurandthenumberofdifferenthabitatsthattheyexploit(egcoralreefsrockyreefsseagrassbedsmangrovesLuizetal2012)Dietaryspecializationisoftendefinedbytheproportionofdifferentfoodcategoriestar-geted (Pratchett 2014)We predict that butterflyfishes endemictotheArabianPeninsularegionwillhavehigherdietaryspecializa-tionandrelianceoncorals forfoodgivenrecentoriginsalongsidetheircoralrichhabitat(Renemaetal2016)Wechoosetofocusonadultversuslarvalecologicaltraitsbecausemoreinformationabouttheformerisavailableandhasbeenshowntocorrelatewithpast(Ottimofioreetal2017)andpresent(Luizetal2013)geographicrangesize
TheaimsofthisstudyarethreefoldFirstweaimtoreconstructthe phylogeny and evolutionary timescale for Red Sea toArabianGulfbutterflyfishesinordertotestwhethertheseperipheralareasintermittentlyseedthebroaderIndo-WestPacificwithbiodiversity(ldquoevolutionary incubatorrdquo hypothesis)Outcomes thatwould allowrejection of this hypothesis include a lack of evidence supportingArabianPeninsular endemic fish lineages giving rise to Indo-WestPacific fish lineagesaswell as restrictedancestral rangesexpand-ing intothisbroaderregionSecondwe looktotesttheextenttowhich butterflyfishmaintained a continuous presence in the RedSeaduringthemajorenvironmentalfluctuationsofthePleistocene(ldquoPleistoceneextirpationrdquohypothesis)Outcomes thatwould allowrejection of this hypothesis include a lack of evidence supportingArabianPeninsularendemicfishoriginatingaftertheglacialcyclesofthePleistoceneaswellascolonizationeventsdatedonlybeforeorafterthisepochThirdweaimtotestwhetherspeciesendemictothecoastalwatersoftheArabianPeninsulanon-randomlyasso-ciatewithparticularecologicaltraits(ldquoecologicaltraitrdquohypothesis)whichmaybeimportantinexplainingpatternsofdiversificationinthis regionTheexpectationhere is that endemic fishes aremorespecialized and thus better adapted to local conditions than theirwidespreadcongenersOutcomesthatwouldallowrejectionofthishypothesisincludealackofassociationbetweenendemismandanyoftheecologicaltraitsconsideredhere
2emsp |emspMATERIAL S AND METHODS
21emsp|emspMaterials
Site location sampling date and museum voucher information(where available) for each specimen are outlined in SupportingInformationTableS1AllbutterflyfishspeciesincludedinthisstudyandtheirgeographicdistributionarelistedinTable1
Asourprimaryobjectiveistoreconstructtheevolutionaryhis-toryofbutterflyfishesknowntooccurintheRedSeaandadjacentgulfsorseasweconcentratedoursamplingeffortsonthosespe-ciesandtheirclosestrelativesAlthoughfivemajorChaetodontidaelineages were sampled Chaetodon Clade CH1 (Chaetodon robus‐tus andC hoefleri restrictedtotheAtlanticCowmanampBellwood2013) andmultiple bannerfish genera (Amphichaetodon Chelmon Chelmonops Coradion Hemitaurichthys and Johnrandallia) withoutspeciesrepresentedintheRedSeawerenotsampledinthisstudyTwospeciesof thePrognathodes genuswere included to facilitatefossilcalibrationbutwerenotincludedinthebiogeographicanaly-sesduetotheirAtlanticdistributions(seebelow)
Intotalwesampled47chaetodontidspecies(35oftheentirefamily)whichincludesallregionalendemicsandwide-rangingspe-ciesfoundintheArabianPeninsularegionsaveRoa jayakariararedeepwaterspeciesdistributedfromtheRedSeatocoastalIndiawewereunable to secure a tissue sample aspartof this studyEightofthesespecieshavenotpreviouslybeensampledinphylogeneticstudiesof the family (Bellwoodetal2010CowmanampBellwood2011FesslerampWestneat2007Hodgeetal2014)Tissueswerepreservedinasaturatedsalt-DMSOsolutionor95ethanolpriortoprocessingThisresearchwascarriedoutunderthegeneralauspicesofKingAbdullahUniversityofScienceandTechnologyrsquos (KAUST)arrangements for marine research with the Saudi Arabian CoastGuard and the Presidency ofMeteorology and Environment TheanimaluseprotocolwasapprovedbyKAUSTrsquosBiosafetyandEthicsCommittee(KAUSTdoesnotprovidespecificapprovalnumber)
22emsp|emspPhylogenomics approach
We employ the sequence capture method of ultraconserved ele-ments(UCEs)toproducemillionsofreadsinparallelfrommultiplebutterflyfishspecimenscollectedfromtheGulfofAqabainthewest(Red Sea) to theHawaiianArchipelago in the east (PacificOceanPO) UCEs are a class of highly conserved and abundant nuclearmarkers distributed throughout the genomes of most organisms(BejeranoHausslerampBlanchette2004Siepeletal2005Renekeretal2012)Thesemarkersdonotintersectparalogousgenes(DertiRothChurchampWu 2006) do not have retro-element insertions(SimonsPheasantMakuninampMattick2006)havearangeofvari-antsites(ieevolvingondifferenttimescalesFairclothetal2012)andhavebeenusedtoreconstructphylogeniesacrossvertebrates(Bejerano et al 2004 Faircloth et al 2012 Faircloth SorensonSantiniampAlfaro2013McCormacketal2013Smithetal2014Sunetal2014)includingfishesatbothshallow(Mcgeeetal2016)
10992emsp |emsp emspensp DIBATTISTA eT Al
TAB
LE 1
emspSpeciesdistributionandcladedesignationfromBellwoodetal(2010)andCowmanandBellwood(2011)forallChaetodontidaesamplesusedinthisstudy
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Clade4
Chae
todo
n au
riga
radicradic
radicradic
radicradic
radicradic
Chae
todo
n au
ripes
radic
Chae
todo
n co
llare
radicradic
radicradic
radicradic
Chae
todo
n de
cuss
atus
radicradic
Chae
todo
n di
aleu
cos
radicradic
Chae
todo
n fa
lcul
aradic
Chae
todo
n fa
scia
tus
radicradic
radic
Chae
todo
n ga
rdin
eri
radicradic
radicradic
radic
Chae
todo
n le
ucop
leur
aradic
radicradic
radicradic
Chae
todo
n lin
eola
tus
radicradic
radicradic
radicradic
Chae
todo
n lu
nula
radicradic
radicradic
radic
Chae
todo
n m
elan
notu
sradic
radicradic
radicradic
radic
Chae
todo
n m
esol
euco
sradic
radicradic
radic
Chae
todo
n ni
grop
unct
atus
radic
radicradic
Chae
todo
n ox
ycep
halu
sradic
radic
Chae
todo
n pi
ctus
radic
radicradic
radicradic
Chae
todo
n se
mila
rvat
us
radicradic
radicradic
Chae
todo
n va
gabu
ndus
radicradic
radic
Clade3
Chae
todo
n au
stria
cus
radicradic
radicradic
Chae
todo
n ba
rone
ssa
radic
Chae
todo
n be
nnet
tiradic
radicradic
Chae
todo
n la
rvat
us
radicradic
radicradic
Chae
todo
n lu
nula
tus
radic
Chae
todo
n m
elap
teru
sradic
radicradic
radicradic
radic
Chae
todo
n pl
ebei
usradic
Chae
todo
n sp
ecul
umradic
radic
Chae
todo
n tr
iang
ulum
radic
Chae
todo
n tr
ifasc
ialis
radicradic
radicradic
radicradic
radic
Chae
todo
n tr
ifasc
iatu
sradic
radicradic
(Con
tinue
s)
emspensp emsp | emsp10993DIBATTISTA eT Al
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Chae
todo
n za
nzib
arie
nsis
radicradic
radic
Clade2
Chae
todo
n gu
ttat
issim
usradic
radic
Chae
todo
n in
terr
uptu
sradic
Chae
todo
n kl
eini
iradic
radicradic
Chae
todo
n m
adag
aska
riens
isradic
Chae
todo
n m
erte
nsii
radic
Chae
todo
n pa
ucifa
scia
tus
radicradic
radic
Chae
todo
n pe
lew
ensis
radic
Chae
todo
n pu
ncta
tofa
scia
tus
radicradic
Chae
todo
n tr
ichr
ous
radic
Chae
todo
n un
imac
ulat
usradic
radic
Chae
todo
n xa
nthu
rus
radic
Bannerfishes
Forc
ipig
er fl
aviss
imus
radicradic
radicradic
radic
Forc
ipig
er lo
ngiro
stris
radicradic
radic
Hen
ioch
us a
cum
inat
usradic
radicradic
radicradic
radicradic
Hen
ioch
us d
iphr
eute
sradic
radicradic
radicradic
radic
Hen
ioch
us in
term
ediu
sradic
radicradic
ColorsinthetableheadermatchthecolorsusedtodenotespeciesdistributionsinFigure1AsterisksindicateregionalendemicsforthepurposesofourcorrelationaltraitanalysisThelettersbeloweach
regionindicatethegeographicgroupingsusedforBioGeoBEARSanalysisAlthoughC
haet
odon
leuc
ople
uraC
haet
odon
mel
aptu
rusand
Chae
todo
n pi
ctusarelistedasbeingpresentintheRedSeathisis
basedonrarerecordsattheirnorthernlimitsSimilarlywehaveonlysampledC
pic
tus(andnotC
haet
odon
vag
abun
dus)atSocotra(DiBattistaetal2017)andrarerecordsofC
haet
odon
aus
tria
cusinthe
GulfofAdenandSouthOmanlikelyrepresentwaifs
TAB
LE 1
emsp(Continued)
10994emsp |emsp emspensp DIBATTISTA eT Al
anddeep(Alfaroetal2018Fairclothetal2013Harringtonetal2016)phylogeneticscales
23emsp|emspDNA library preparation and next‐generation sequencing
DNA was extracted with DNeasy Blood and Tissue kits (QiagenValenciaCA)whichincludedanRNAseAtreatmentstepEachex-tractedsamplewasvisualizedbygelelectrophoresistoassessDNAqualityTotalDNAfromeachextractedaliquotwasquantifiedusingaQubitdsDNAHSAssayKit(InvitrogenCarlsbadCA)and12microgofDNAperindividualsamplewasfragmentedbysonicationto500basepairs (bp)usingaCovarisS2 sonicator (Covaris IncWoburnMA)andusedforUCElibrarypreparationInbriefweend-repairedadenylated and ligated fragmentedDNA to Illumina TruSeq-styleadapters which included custom sequence tags to barcode eachindividualsample (FairclothampGlenn2012)Followingan18-cyclePCRtoamplify indexed libraries forenrichmentwecreatedpoolsbycombining625ngofeightindividuallibrariesEachpoolwascon-centratedto147ngμlusingavacuumcentrifugeWethenfollowedanestablishedworkflowfortargetenrichment(Gnirkeetal2009)withmodificationsspecifiedinFairclothetal(2012)SpecificallyweenrichedeachpooltargetingUCElociandtheirflankingsequenceusingsyntheticRNAcaptureprobes(MyBaitsMycroarrayIncAnnArborMI)We combined the enriched indexed pools at equimo-lar ratios prior to sequencing The two final pooled librarieswereeach runpaired-end (150bpsequencing)on independent lanesofanIlluminaHiSeq2000(v3reagents)attheKAUSTBioscienceCoreLabDetailedmethodsoflibraryenrichmentpost-enrichmentPCRandvalidationusingrelativeqPCRmaybefoundathttpsultracon-servedorgprotocols
24emsp|emspSequence read quality control assembly and UCE identification
Weremovedadaptercontaminationand lowqualitybaseswith il-lumiprocessor (Faircloth2013)aparallelwrappertoTrimmomatic(BolgerLohseampUsadel2014)ToassemblethetrimmeddatasetweusedthePHYLUCEpipeline (version8ca5884Faircloth2016)with the phyluce_assembly_assemblo_trinitypywrapper script forTrinity(version150Grabherretal2011)WematchedassembledcontigstoenrichedUCElocibyaligningcontigsfromeachspeciesto our UCE probes using the phyluce_assembly_match_contigs_to_probespy scriptwith the LASTZ assembler (Harris 2007)WestoredthesematchresultsintoaSQLiterelationaldatabaseafterex-cludingcontigsthatmatchedmultipleUCElociandUCElociwhoseprobesmatchedmultiplecontigs
Weusedphyluce_align_seqcappytoalignUCElociwithMAFFT(Katohamp Standley 2013KatohMisawaKumaampMiyata 2002)Following alignment we end- and internally-trimmed alignmentswithGBLOCKS (Castresana 2000) to improvephylogenetic infer-encebyremovingpoorlyalignedorhighlydivergentsites(TalaveraampCastresana2007)Weselectedlocithatwerepresentinatleast
75 of our specimens and concatenated the alignments into aPHYLIP-formatted matrix for phylogenetic analysis We includedpreviouslypublishedUCEdataforthreespeciesinouralignmenttorepresentAcanthomorpha outgroup lineages andmore accuratelycalibratethephylogeny(seebelow)
25emsp|emspPhylogenetic analysis of concatenated UCE data evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
WefullypartitionedourconcatenatedalignmentbyUCElocusandperformedBayesiananalysesofthedatasetwithExaBayes(AbererKobert amp Stamatakis 2014) and two independent runs samplingevery500generationsWeusedtheautostoppingconvergencecri-teriaof anaverage standarddeviationof split frequenciesoflt5and visualized the log-likelihood of each chain to ensure conver-genceinTracerversion16(Rambautetal2014)
WeestimateddivergencetimesusingMCMCTREEinthePAMLpackage on the Bayesian consensus topologyWe used the likeli-hood approximation approach following the two-step proceduredescribedbyDosReis andYang (2011) by first estimating ameansubstitutionratefortheentirealignmentwithBASEMLunderastrictmolecularclockandthenusingthisestimatetosetthergene_priorinMCMCTREEWeusedasingleunpartitionedalignmentforcom-putationaltractabilitywithanHKY85modelfivecategoriesforthegammadistributionofrateheterogeneityanrgene_gammapriorforthe gamma distribution describing gene rate heterogeneity of (237105751)andasigma2_gammapriorof (251)WeadoptedacalibrationstrategythatbuildsonHarringtonetal(2016)byinclud-ingmoreproximalacanthomorphoutgroupstoChaetodontidaeandtheirimmediaterelativesWeconstrainedsixnodesonthebasisoffossilinformationusinghardlowerandsoftupperboundsoutlinedinSupportingInformationFigureS1Weassignedaminimumamountofpriorweightforagesbelowthelowerbound(1e-200)and5priorweightforageshigherthantheupperboundBrieflywelinkaseriesofcarangimorphsyngnathiformholocentroidandlampridiformfossilstothesequencesofacanthomorphoutgroupfossilsasperHarringtonet al (2016) This resulted in the following outgroup node calibra-tions acanthuroids versus all other taxa (lower bound 5417Maupperbound7084Ma)acanthuridsversuszanclids (lowerbound490Ma upper bound 627Ma) Naso versus Acanthurus (lowerbound 490Ma upper bound 5722Ma) Chaetodontidae versusPomacanthidae (lower bound 2962Ma upper bound 5926Ma)and the total-group Chaetodon versus Prognathodes (lower bound7Maupperbound475Ma)FurtherjustificationforcalibrationsisavailableasSupportingInformation(AppendixS1)
26emsp|emspAncestral biogeographic range estimation evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Weestimatedancestraldistributionpatterns forchaetodontid lin-eages using the pruned time-calibrated phylogeny analyzed with
emspensp emsp | emsp10995DIBATTISTA eT Al
theRpackageBioGeoBEARS(Matzke2013)whichallowsseveralmodels of biogeographic evolution to be compared via likelihoodinference and the ability to incorporate a parameter allowing forfounder-eventspeciationFortheseanalyseswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareasGulfofAqabarestoftheRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPOThediscretecodingofgeographicareasadjacenttotheArabianPeninsulaenablesafine-scaleinvestigationoftheances-tralbiogeographyofthatregionforourtaxaofinterestPresenceabsenceandgeographicalrangedataforeachtaxonwereobtainedfromacombinationofDiBattistaRobertsetal(2016)andFishBase(FroeseampPauly2011)Prognathodesspp(aChaetodontidaegenus)werenotconsideredinthispartoftheanalysisgiventhatthesetwotaxaarerestrictedtotropicalAtlanticwaters
Weconstrainedourbiogeographicanalysestoprohibitcoloniza-tioneventsbetweentheRedSeaandIndianPOregionsbefore5Mareflectingthetimewhenamorepermanentconnectionwasformedvia theStraitofBabalMandab (Bailey2010)OurBioGeoBEARSanalysis evaluated the DEC DIVALIKE and BAYAREALIKE mod-elswithandwithoutthejump(J)parameter(Matzke2013)Thesemodels describe biogeographic scenarios where dispersal extinc-tioncladogenesisvicarianceandfoundereventsaredifferentiallyinvokedtoexplainpresentdaydistributionalpatterns Inourcasewewereinterestedinwhethertherange-restrictedendemicsfromthecoastalwatersoftheArabianPeninsularepresentancientrelictsnew colonization events andor a sourceof biodiversity (at somepointinthepast)forthebroaderIndo-WestPacific
27emsp|emspComparative trait analysis evaluation of the ldquoecological traitrdquo hypothesis
In order to determine whether particular species-level traitswere associatedwith the evolutionof endemism in this subset ofChaetodontidaespecieswefittedaphylogeneticgeneralizedlinearmodel(functionldquophyloglmrdquoinRpackageldquophylolmrdquo[Hoetal2016])thatassumedldquoregionalendemismrdquo(ieendemictothecoastalwa-tersoftheArabianPeninsulaDiBattistaRobertsetal2016)asthebinomialresponsevariableandasuiteofecologicaltraitsasthepre-dictivefixedfactorsFormodelselectionweperformedabackwardstepwiseprocedureforPGLMrsquos(functionldquophylosteprdquoinRpackageldquophylolmrdquo[Hoetal2016])whichentailedsequentialoptimizationbyremovingnon-influentialfixed-effecttermsfromthefullmodelbasedonAkaikeinformationcriteria(AIC)Fulldetailsonthemeth-odsanddatasourcesareprovidedinSupportingInformationTableS2Wealsoexplore interactionsamongthepredictivetraitsusinga regression tree approach (Dersquoath and Fabricius 2000 functionldquorpartrdquoinRpackageldquorpartrdquo[Therneauetal2015])
Amongthepredictivevariablesconsideredweremaximumbodysize(totallength=TLAllenetal1998Kuiter2002)depthrangeinhabited (Allenet al1998) social structure (threecategoriesor-deredfromlowtohighsociabilitysolitarypairformationandgroupformation Allen et al 1998 Kuiter 2002 Yabuta and Berumen
2013) habitat breadth (estimated as the sum value of all habitattypes inhabited C=coral R=rocky D=deep reef S=sedimentR=rubbleCO=coastalCA=algalbedsAllenetal1998Kuiter2002)anddietaryrelianceoncoral reefs (fourcategoriesorderedfromlowtohighrelianceplanktivorebenthicinvertivorefaculta-tivecorallivoreandobligatecorallivoreColeandPratchett2014)Wealsoincludedthephylogeneticageofspecies(Myr)asanaddi-tional fixedfactor totestwhetherspecies traitsare influencedbytimeofdivergencefromsistertaxaForphylogeneticageweeval-uate for each species (regional endemic andwidespread)whetherwe sampled its closest sister speciesby comparingourphylogenywith those published previously (CowmanampBellwood 2011) andotherpublishedaccounts(Kuiter2002)Theecologicaltraitswereselected because they are associated with specialization fitnessandrangeexpansioninbutterflyfishesandthusmayhelptoexplainpatternsofevolutioninfishendemictothecoralreefsoftheArabianPeninsulaWedonotethismaybeanoversimplificationgiventhatourcategoriesarecoarseandbiasedtowardadultversuslarvaltraitswhichare themselvesdatadeficientPreviousworkhoweverhasdemonstratedthattraitsassociatedwiththesuccessfulrecruitmentofreeffisharemoreimportantthantraitsassociatedwithdispersalindeterminingdifferentiationbetweenhabitats(Gaitheretal2015KeithWoolseyMadinByrneampBaird2015)
3emsp |emspRESULTS
31emsp|emspUCE sequences
ReadscontigsandUCElociperindividualareoutlinedinSupportingInformationTableS3Insummarywesequencedatotalof15331millionreadswithameanof155millionreadspersamplefrom47focaltaxa(excludingoutgroupsalsoseeTable1)Overallweassem-bledameanof12969contigs(95CImin=10593max=15345)and901UCElocipersample(95CImin=871max=932)
32emsp|emspPhylogenetic reconstruction and timing of divergence evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Followingassemblyalignmenttrimmingandfilteringoutlocithatwerepresentinfewerthan75specimens(fora75completedata-set)we retained971 alignmentswith amean length of 5156bpThe concatenated supermatrix contained500642bpwith52680informativesitesandwas833completebasedontheproportionofnon-gapsequencesThefollowingsampleswereexcludedfromfurtheranalysisduetothelownumberoflocirecoveredChaetodon_interruptus1a Chaetodon_lineolatus1a Chaetodon_lunula1a andChaetodon ulietensis1a (for full details see Supporting InformationTableS1) however tissue replicateswere retained for twoof thefourspecieslistedhere(Chaetodon lineolatusandChaetodon lunula)
Our Bayesian and maximum likelihood analyses produced afully resolvedtopologythatsharedkeypointsofcongruencewithpriormulti-locus studies of butterflyfishes (Bellwood et al 2010
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
AbererA JKobertKampStamatakisA (2014)ExaBayesMassivelyparallelBayesiantreeinferenceforthewhole-genomeeraMolecular Biology and Evolution 31 2553ndash2556 httpsdoiorg101093molbevmsu236
AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
Ecology and Evolution 2018810989ndash11008 emsp|emsp10989wwwecolevolorg
Received12May2018emsp |emsp Revised19August2018emsp |emsp Accepted29August2018DOI 101002ece34566
O R I G I N A L R E S E A R C H
Ice ages and butterflyfishes Phylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot
Joseph D DiBattista123 emsp|emspMichael E Alfaro4emsp|emspLaurie Sorenson4emsp|emspJohn H Choat5emsp|emsp Jean‐Paul A Hobbs3emsp|emspTane H Sinclair‐Taylor1emsp|emspLuiz A Rocha6emsp|emspJonathan Chang4 emsp|emsp Osmar J Luiz7emsp|emspPeter F Cowman8emsp|emspMatt Friedman910emsp|emspMichael L Berumen1
1RedSeaResearchCenterDivisionofBiologicalandEnvironmentalScienceandEngineeringKingAbdullahUniversityofScienceandTechnologyThuwalSaudiArabia2AustralianMuseumResearchInstituteAustralianMuseumSydneyNewSouthWalesAustralia3SchoolofMolecularandLifeSciencesCurtinUniversityPerthWesternAustraliaAustralia4DepartmentofEcologyandEvolutionaryBiologyUniversityofCaliforniaLosAngelesLosAngelesCalifornia5CollegeofScienceandEngineeringJamesCookUniversityTownsvilleQueenslandAustralia6SectionofIchthyologyCaliforniaAcademyofSciencesSanFranciscoCalifornia7ResearchInstitutefortheEnvironmentandLivelihoodsCharlesDarwinUniversityDarwinNorthernTerritoryAustralia8ARCCentreofExcellenceforCoralReefStudiesJamesCookUniversityTownsvilleQueenslandAustralia9DepartmentofEarthSciencesUniversityofOxfordOxfordUK10MuseumofPaleontologyandDepartmentofEarthandEnvironmentalSciencesUniversityofMichiganAnnArborMichigan
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd
CorrespondenceJosephDDiBattistaAustralianMuseumResearchInstituteAustralianMuseumSydneyNSWAustraliaEmailjosephdibattistagmailcom
Funding informationKAUSTOfficeofCompetitiveResearchFundsGrantAwardNumberCRG-1-2012-BER-002AustralianResearchCouncilGrantAwardNumberDE170100516NationalGeographicSocietyGrantAwardNumber9024-11NationalScienceFoundationGrantAwardNumberDE170100516
AbstractFortropicalmarinespecieshotspotsofendemismoccurinperipheralareasfurthestfromthecenterofdiversitybuttheevolutionaryprocessesthatleadtotheiroriginremain elusiveWe test several hypotheses related to the evolutionof peripheralendemicsbysequencingultraconservedelement (UCE) locitoproduceagenome-scalephylogenyof47butterflyfishspecies(familyChaetodontidae)thatincludesallshallowwaterbutterflyfishfromthecoastalwatersoftheArabianPeninsula(ieRedSeatoArabianGulf)andtheircloserelativesBayesiantreebuildingmethodspro-ducedawell-resolvedphylogenythatelucidatedtheoriginsofbutterflyfishesinthishotspotsofendemismWeshowthatUCEsoftenusedtoresolvedeepevolutionaryrelationshipsrepresentanimportanttooltoassessthemechanismsunderlyingre-centlydivergedtaxaOuranalysesindicatethatuniqueenvironmentalconditionsinthecoastalwatersoftheArabianPeninsulaprobablycontributedtotheformationofendemicbutterflyfishesOlderendemicspeciesarealsoassociatedwithnarrowver-sus broad depth ranges suggesting that adaptation to deeper coral reefs in thisregionoccurredonlyrecently(lt175Ma)Eventhoughdeepreefenvironmentswere
10990emsp |emsp emspensp DIBATTISTA eT Al
1emsp |emspINTRODUC TION
Explaining the underlying factors responsible for the diversity ofspecies accumulated at hotspots of endemism remains a difficultprobleminthefieldofbiogeographyRecentresearchhasidentifiedtheimportanceofperipheralregionsfromtropicaloceansingener-atingandexportingbiologicaldiversitythusintermittentlyseedingadjacent seas (BowenRocha ToonenampKarl 2013DiBattista etal2013DiBattistaWilcoxCraigRochaampBowen2010Ebleetal2011Gaitheretal2011GaitherToonenRobertsonPlanesampBowen2010MalayampPaulay2010SkillingsBirdampToonen2010)howeverdirecttestsofthisassumptionarerareRenewedinterestin theRedSea toArabianGulf (orPersianGulf) regionprovidesanew opportunity to explore hypotheses associated with how en-demicsareformedinperipheralareasanditspotentialcontributiontothespeciesrichnessofmarinebiodiversityhotspotsTheRedSeaisasemi-enclosedbasinlocatedatthenorth-westerncorneroftheIndianOceanandharborsoneofthehighestlevelsofendemismformarineorganisms(129forfishes126forpolychaetes81forechinoderms 165 for ascidians and 58 for scleractinian cor-alsDiBattistaRobertsetal2016)Thelevelofendemismamongwell-characterizedgroupsintheRedSeasuchastheshorefishesexceedsthoseofallotherperipheralendemichotspotsidentifiedfortheIndianOcean(DiBattistaRobertsetal2016)AlthoughmanyoftheseRedSeaendemicsextendtheirdistribution intotheadja-centGulfofAdenandArabianSea(DiBattistaChoatetal2016DiBattistaRobertsetal2016Kemp1998)itisnotclearwhethertheyarepaleo-endemics(oldlineagesrestrictedduetorangecon-traction) neo-endemics (young lineages at the site of origin) orldquoecologicalrdquoendemics(oldoryounglineageswitharestrictedrangeduetospeciesecologyseeCowmanParraviciniKulbickiampFloeter2017)andwherewhenandhowthisdiversificationoccurred
TheRedSeahasauniquegeologicalandpaleoclimatichistorythatmayhaveplayedaroleinitshighlevelsofendemism(seeDiBattistaChoatetal2016forreview)InbrieftheRedSeabasinwasformedbyepisodesofseafloorspreading41ndash34Ma(GirdlerampStyles1974)followedby intermittentconnections to theMediterraneanSea inthe north (~14ndash5MaHubert-Ferrari et al 2003) and amore re-centconnectiontotheGulfofAdeninthesouththroughtheStraitofBabalMandab (~5Ma topresentBailey2010)TheStrait isanarrowchannel (29km)withashallowsill (137m)thatconstitutesthe only connection between the Red Sea and the Indian Ocean
(Bailey2010)Waterexchange is regulatedby IndianOceanmon-soonpatterns(RaitsosPradhanBrewinStenchikovampHoteit2013Smeed1997)butwashistoricallyminimalorabsentduringreducedsealevelscausedbyglacialperiodsofthePleistocene(Rohlingetal2009)includingthemostrecentglacialmaximum(20ndash15kaLudtampRocha2015Siddalletal2003)RestrictedwaterflowresultedinincreasedsalinitywithintheRedSea(BitonGildorampPeltier2008)leadingsometosuggestthattherewascompleteextirpationofRedSeafaunaduringtheseperiods(Klausewitz1989)TheldquoPleistoceneextirpationrdquohypothesiswhereinallRedSeafaunawereeliminatedduringthe lastglacialmaximum(~18ka)andsubsequentlyre-pop-ulated via more recent colonization events remains controversialand untested with modern comparative approaches (DiBattistaChoatetal2016)althoughsimilargeologicaleventsmayhaveoc-curredintheMediterraneanSea(Bianchietal2012)Thusdespitesomeagreementonthebroadstrokesof itsgeologichistory littleconsensushasemergedontheprocessesthatshapedtheArabianPeninsularsquospresentdaymarinebiodiversitytheirinfluenceonbiodi-versityinadjacentregionsandtheroleofhistoricalclosuresoftheStraitofBabalMandab
ButterflyfishesandbannerfishesbrightlycoloredreeffishesinthefamilyChaetodontidaeareapotentialmodelsystemforeluci-datingtheoriginsmaintenanceandevolutionaryhistoryofRedSeaendemicsandtheirinfluenceonspeciesrichnessinadjacentmarineregionsThefamily isdiverse (17species intheRedSeaandgt130species in the greater Indo-West Pacific Allen Steene amp Allen1998)andphylogeneticallywellresolvedcomparedtootherreeffishfamilies(Cowman2014)AhighproportionoftheChaetodontidaespecies found in the coastal waters of the Arabian Peninsula areendemic (32 DiBattista Roberts et al 2016) Although recentmolecularphylogeniesofchaetodontidshavehelpedtoclarifymanyaspectsoftheirevolutionaryhistory(Bellwoodetal2010Cowmanamp Bellwood 2011 2013 Fessler amp Westneat 2007 HodgeHerwerdenampBellwood2014HsuChenampShao2007)alackofsamplingofArabianPeninsulaspecieshasimpededourunderstand-ingofthediversificationinthisregion
Theevolutionofendemicspecieshasbeenlinkedtoecologicaltraits such as reductions indispersal ability and changes inbodysize(ietheislandrulereviewedbyLomolino2005WhittakerandFernaacutendez-Palacios2007)Forreeffishescertaintraitsassociatedwith dispersal ability are linked to geographic range size For ex-amplelargegregariousandnocturnalspeciestendtohavelarger
drasticallyreducedduringtheextremelowsealevelstandsofglacialagesshallowreefspersistedandassuchtherewasnoevidencesupportingmassextirpationoffaunainthisregion
K E Y W O R D S
biogeographicbarriersChaetodoncoralreefglaciationeventsPleistoceneultraconservedelements
emspensp emsp | emsp10991DIBATTISTA eT Al
rangesizesthansmallsolitaryandstrictlydiurnalspecies(Luizetal20132012)Moreoverdispersalabilitycanpotentiallyinfluencecladediversificationtosuccessfullycolonizeandestablishpopula-tionsinperipheralareastropicalfishspeciesmustbegooddispers-ers(HobbsJonesMundayConnollyampSrinivasan2012)Followingdiversification in peripheral areas newly formed lineages mayevolvetraitslessconducivetodispersalthusbecomingendemictotheareawhereitoriginatedasoftenoccursintheevolutionofinsu-larterrestrialendemics(WhittakerandFernaacutendez-Palacios2007)We thereforepredict thatbutterflyfishesendemic to theArabianPeninsularegionwillhavesmallerbodysizeshighersociabilityandreduceddispersalabilitycomparedtotheirwidespreadcongenersBroadly speaking endemic species tend to be ecological special-istsandthusadaptedtotheenvironmentalconditioninwhichtheyarose (McKinney 1997) We therefore additionally predict thattheseendemicswillhaveahigherlevelofecologicalspecializationthanwidespread species For reef fishes habitat specialization isoftendefinedbythedepthrangewheretheyoccurandthenumberofdifferenthabitatsthattheyexploit(egcoralreefsrockyreefsseagrassbedsmangrovesLuizetal2012)Dietaryspecializationisoftendefinedbytheproportionofdifferentfoodcategoriestar-geted (Pratchett 2014)We predict that butterflyfishes endemictotheArabianPeninsularegionwillhavehigherdietaryspecializa-tionandrelianceoncorals forfoodgivenrecentoriginsalongsidetheircoralrichhabitat(Renemaetal2016)Wechoosetofocusonadultversuslarvalecologicaltraitsbecausemoreinformationabouttheformerisavailableandhasbeenshowntocorrelatewithpast(Ottimofioreetal2017)andpresent(Luizetal2013)geographicrangesize
TheaimsofthisstudyarethreefoldFirstweaimtoreconstructthe phylogeny and evolutionary timescale for Red Sea toArabianGulfbutterflyfishesinordertotestwhethertheseperipheralareasintermittentlyseedthebroaderIndo-WestPacificwithbiodiversity(ldquoevolutionary incubatorrdquo hypothesis)Outcomes thatwould allowrejection of this hypothesis include a lack of evidence supportingArabianPeninsular endemic fish lineages giving rise to Indo-WestPacific fish lineagesaswell as restrictedancestral rangesexpand-ing intothisbroaderregionSecondwe looktotesttheextenttowhich butterflyfishmaintained a continuous presence in the RedSeaduringthemajorenvironmentalfluctuationsofthePleistocene(ldquoPleistoceneextirpationrdquohypothesis)Outcomes thatwould allowrejection of this hypothesis include a lack of evidence supportingArabianPeninsularendemicfishoriginatingaftertheglacialcyclesofthePleistoceneaswellascolonizationeventsdatedonlybeforeorafterthisepochThirdweaimtotestwhetherspeciesendemictothecoastalwatersoftheArabianPeninsulanon-randomlyasso-ciatewithparticularecologicaltraits(ldquoecologicaltraitrdquohypothesis)whichmaybeimportantinexplainingpatternsofdiversificationinthis regionTheexpectationhere is that endemic fishes aremorespecialized and thus better adapted to local conditions than theirwidespreadcongenersOutcomesthatwouldallowrejectionofthishypothesisincludealackofassociationbetweenendemismandanyoftheecologicaltraitsconsideredhere
2emsp |emspMATERIAL S AND METHODS
21emsp|emspMaterials
Site location sampling date and museum voucher information(where available) for each specimen are outlined in SupportingInformationTableS1AllbutterflyfishspeciesincludedinthisstudyandtheirgeographicdistributionarelistedinTable1
Asourprimaryobjectiveistoreconstructtheevolutionaryhis-toryofbutterflyfishesknowntooccurintheRedSeaandadjacentgulfsorseasweconcentratedoursamplingeffortsonthosespe-ciesandtheirclosestrelativesAlthoughfivemajorChaetodontidaelineages were sampled Chaetodon Clade CH1 (Chaetodon robus‐tus andC hoefleri restrictedtotheAtlanticCowmanampBellwood2013) andmultiple bannerfish genera (Amphichaetodon Chelmon Chelmonops Coradion Hemitaurichthys and Johnrandallia) withoutspeciesrepresentedintheRedSeawerenotsampledinthisstudyTwospeciesof thePrognathodes genuswere included to facilitatefossilcalibrationbutwerenotincludedinthebiogeographicanaly-sesduetotheirAtlanticdistributions(seebelow)
Intotalwesampled47chaetodontidspecies(35oftheentirefamily)whichincludesallregionalendemicsandwide-rangingspe-ciesfoundintheArabianPeninsularegionsaveRoa jayakariararedeepwaterspeciesdistributedfromtheRedSeatocoastalIndiawewereunable to secure a tissue sample aspartof this studyEightofthesespecieshavenotpreviouslybeensampledinphylogeneticstudiesof the family (Bellwoodetal2010CowmanampBellwood2011FesslerampWestneat2007Hodgeetal2014)Tissueswerepreservedinasaturatedsalt-DMSOsolutionor95ethanolpriortoprocessingThisresearchwascarriedoutunderthegeneralauspicesofKingAbdullahUniversityofScienceandTechnologyrsquos (KAUST)arrangements for marine research with the Saudi Arabian CoastGuard and the Presidency ofMeteorology and Environment TheanimaluseprotocolwasapprovedbyKAUSTrsquosBiosafetyandEthicsCommittee(KAUSTdoesnotprovidespecificapprovalnumber)
22emsp|emspPhylogenomics approach
We employ the sequence capture method of ultraconserved ele-ments(UCEs)toproducemillionsofreadsinparallelfrommultiplebutterflyfishspecimenscollectedfromtheGulfofAqabainthewest(Red Sea) to theHawaiianArchipelago in the east (PacificOceanPO) UCEs are a class of highly conserved and abundant nuclearmarkers distributed throughout the genomes of most organisms(BejeranoHausslerampBlanchette2004Siepeletal2005Renekeretal2012)Thesemarkersdonotintersectparalogousgenes(DertiRothChurchampWu 2006) do not have retro-element insertions(SimonsPheasantMakuninampMattick2006)havearangeofvari-antsites(ieevolvingondifferenttimescalesFairclothetal2012)andhavebeenusedtoreconstructphylogeniesacrossvertebrates(Bejerano et al 2004 Faircloth et al 2012 Faircloth SorensonSantiniampAlfaro2013McCormacketal2013Smithetal2014Sunetal2014)includingfishesatbothshallow(Mcgeeetal2016)
10992emsp |emsp emspensp DIBATTISTA eT Al
TAB
LE 1
emspSpeciesdistributionandcladedesignationfromBellwoodetal(2010)andCowmanandBellwood(2011)forallChaetodontidaesamplesusedinthisstudy
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Clade4
Chae
todo
n au
riga
radicradic
radicradic
radicradic
radicradic
Chae
todo
n au
ripes
radic
Chae
todo
n co
llare
radicradic
radicradic
radicradic
Chae
todo
n de
cuss
atus
radicradic
Chae
todo
n di
aleu
cos
radicradic
Chae
todo
n fa
lcul
aradic
Chae
todo
n fa
scia
tus
radicradic
radic
Chae
todo
n ga
rdin
eri
radicradic
radicradic
radic
Chae
todo
n le
ucop
leur
aradic
radicradic
radicradic
Chae
todo
n lin
eola
tus
radicradic
radicradic
radicradic
Chae
todo
n lu
nula
radicradic
radicradic
radic
Chae
todo
n m
elan
notu
sradic
radicradic
radicradic
radic
Chae
todo
n m
esol
euco
sradic
radicradic
radic
Chae
todo
n ni
grop
unct
atus
radic
radicradic
Chae
todo
n ox
ycep
halu
sradic
radic
Chae
todo
n pi
ctus
radic
radicradic
radicradic
Chae
todo
n se
mila
rvat
us
radicradic
radicradic
Chae
todo
n va
gabu
ndus
radicradic
radic
Clade3
Chae
todo
n au
stria
cus
radicradic
radicradic
Chae
todo
n ba
rone
ssa
radic
Chae
todo
n be
nnet
tiradic
radicradic
Chae
todo
n la
rvat
us
radicradic
radicradic
Chae
todo
n lu
nula
tus
radic
Chae
todo
n m
elap
teru
sradic
radicradic
radicradic
radic
Chae
todo
n pl
ebei
usradic
Chae
todo
n sp
ecul
umradic
radic
Chae
todo
n tr
iang
ulum
radic
Chae
todo
n tr
ifasc
ialis
radicradic
radicradic
radicradic
radic
Chae
todo
n tr
ifasc
iatu
sradic
radicradic
(Con
tinue
s)
emspensp emsp | emsp10993DIBATTISTA eT Al
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Chae
todo
n za
nzib
arie
nsis
radicradic
radic
Clade2
Chae
todo
n gu
ttat
issim
usradic
radic
Chae
todo
n in
terr
uptu
sradic
Chae
todo
n kl
eini
iradic
radicradic
Chae
todo
n m
adag
aska
riens
isradic
Chae
todo
n m
erte
nsii
radic
Chae
todo
n pa
ucifa
scia
tus
radicradic
radic
Chae
todo
n pe
lew
ensis
radic
Chae
todo
n pu
ncta
tofa
scia
tus
radicradic
Chae
todo
n tr
ichr
ous
radic
Chae
todo
n un
imac
ulat
usradic
radic
Chae
todo
n xa
nthu
rus
radic
Bannerfishes
Forc
ipig
er fl
aviss
imus
radicradic
radicradic
radic
Forc
ipig
er lo
ngiro
stris
radicradic
radic
Hen
ioch
us a
cum
inat
usradic
radicradic
radicradic
radicradic
Hen
ioch
us d
iphr
eute
sradic
radicradic
radicradic
radic
Hen
ioch
us in
term
ediu
sradic
radicradic
ColorsinthetableheadermatchthecolorsusedtodenotespeciesdistributionsinFigure1AsterisksindicateregionalendemicsforthepurposesofourcorrelationaltraitanalysisThelettersbeloweach
regionindicatethegeographicgroupingsusedforBioGeoBEARSanalysisAlthoughC
haet
odon
leuc
ople
uraC
haet
odon
mel
aptu
rusand
Chae
todo
n pi
ctusarelistedasbeingpresentintheRedSeathisis
basedonrarerecordsattheirnorthernlimitsSimilarlywehaveonlysampledC
pic
tus(andnotC
haet
odon
vag
abun
dus)atSocotra(DiBattistaetal2017)andrarerecordsofC
haet
odon
aus
tria
cusinthe
GulfofAdenandSouthOmanlikelyrepresentwaifs
TAB
LE 1
emsp(Continued)
10994emsp |emsp emspensp DIBATTISTA eT Al
anddeep(Alfaroetal2018Fairclothetal2013Harringtonetal2016)phylogeneticscales
23emsp|emspDNA library preparation and next‐generation sequencing
DNA was extracted with DNeasy Blood and Tissue kits (QiagenValenciaCA)whichincludedanRNAseAtreatmentstepEachex-tractedsamplewasvisualizedbygelelectrophoresistoassessDNAqualityTotalDNAfromeachextractedaliquotwasquantifiedusingaQubitdsDNAHSAssayKit(InvitrogenCarlsbadCA)and12microgofDNAperindividualsamplewasfragmentedbysonicationto500basepairs (bp)usingaCovarisS2 sonicator (Covaris IncWoburnMA)andusedforUCElibrarypreparationInbriefweend-repairedadenylated and ligated fragmentedDNA to Illumina TruSeq-styleadapters which included custom sequence tags to barcode eachindividualsample (FairclothampGlenn2012)Followingan18-cyclePCRtoamplify indexed libraries forenrichmentwecreatedpoolsbycombining625ngofeightindividuallibrariesEachpoolwascon-centratedto147ngμlusingavacuumcentrifugeWethenfollowedanestablishedworkflowfortargetenrichment(Gnirkeetal2009)withmodificationsspecifiedinFairclothetal(2012)SpecificallyweenrichedeachpooltargetingUCElociandtheirflankingsequenceusingsyntheticRNAcaptureprobes(MyBaitsMycroarrayIncAnnArborMI)We combined the enriched indexed pools at equimo-lar ratios prior to sequencing The two final pooled librarieswereeach runpaired-end (150bpsequencing)on independent lanesofanIlluminaHiSeq2000(v3reagents)attheKAUSTBioscienceCoreLabDetailedmethodsoflibraryenrichmentpost-enrichmentPCRandvalidationusingrelativeqPCRmaybefoundathttpsultracon-servedorgprotocols
24emsp|emspSequence read quality control assembly and UCE identification
Weremovedadaptercontaminationand lowqualitybaseswith il-lumiprocessor (Faircloth2013)aparallelwrappertoTrimmomatic(BolgerLohseampUsadel2014)ToassemblethetrimmeddatasetweusedthePHYLUCEpipeline (version8ca5884Faircloth2016)with the phyluce_assembly_assemblo_trinitypywrapper script forTrinity(version150Grabherretal2011)WematchedassembledcontigstoenrichedUCElocibyaligningcontigsfromeachspeciesto our UCE probes using the phyluce_assembly_match_contigs_to_probespy scriptwith the LASTZ assembler (Harris 2007)WestoredthesematchresultsintoaSQLiterelationaldatabaseafterex-cludingcontigsthatmatchedmultipleUCElociandUCElociwhoseprobesmatchedmultiplecontigs
Weusedphyluce_align_seqcappytoalignUCElociwithMAFFT(Katohamp Standley 2013KatohMisawaKumaampMiyata 2002)Following alignment we end- and internally-trimmed alignmentswithGBLOCKS (Castresana 2000) to improvephylogenetic infer-encebyremovingpoorlyalignedorhighlydivergentsites(TalaveraampCastresana2007)Weselectedlocithatwerepresentinatleast
75 of our specimens and concatenated the alignments into aPHYLIP-formatted matrix for phylogenetic analysis We includedpreviouslypublishedUCEdataforthreespeciesinouralignmenttorepresentAcanthomorpha outgroup lineages andmore accuratelycalibratethephylogeny(seebelow)
25emsp|emspPhylogenetic analysis of concatenated UCE data evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
WefullypartitionedourconcatenatedalignmentbyUCElocusandperformedBayesiananalysesofthedatasetwithExaBayes(AbererKobert amp Stamatakis 2014) and two independent runs samplingevery500generationsWeusedtheautostoppingconvergencecri-teriaof anaverage standarddeviationof split frequenciesoflt5and visualized the log-likelihood of each chain to ensure conver-genceinTracerversion16(Rambautetal2014)
WeestimateddivergencetimesusingMCMCTREEinthePAMLpackage on the Bayesian consensus topologyWe used the likeli-hood approximation approach following the two-step proceduredescribedbyDosReis andYang (2011) by first estimating ameansubstitutionratefortheentirealignmentwithBASEMLunderastrictmolecularclockandthenusingthisestimatetosetthergene_priorinMCMCTREEWeusedasingleunpartitionedalignmentforcom-putationaltractabilitywithanHKY85modelfivecategoriesforthegammadistributionofrateheterogeneityanrgene_gammapriorforthe gamma distribution describing gene rate heterogeneity of (237105751)andasigma2_gammapriorof (251)WeadoptedacalibrationstrategythatbuildsonHarringtonetal(2016)byinclud-ingmoreproximalacanthomorphoutgroupstoChaetodontidaeandtheirimmediaterelativesWeconstrainedsixnodesonthebasisoffossilinformationusinghardlowerandsoftupperboundsoutlinedinSupportingInformationFigureS1Weassignedaminimumamountofpriorweightforagesbelowthelowerbound(1e-200)and5priorweightforageshigherthantheupperboundBrieflywelinkaseriesofcarangimorphsyngnathiformholocentroidandlampridiformfossilstothesequencesofacanthomorphoutgroupfossilsasperHarringtonet al (2016) This resulted in the following outgroup node calibra-tions acanthuroids versus all other taxa (lower bound 5417Maupperbound7084Ma)acanthuridsversuszanclids (lowerbound490Ma upper bound 627Ma) Naso versus Acanthurus (lowerbound 490Ma upper bound 5722Ma) Chaetodontidae versusPomacanthidae (lower bound 2962Ma upper bound 5926Ma)and the total-group Chaetodon versus Prognathodes (lower bound7Maupperbound475Ma)FurtherjustificationforcalibrationsisavailableasSupportingInformation(AppendixS1)
26emsp|emspAncestral biogeographic range estimation evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Weestimatedancestraldistributionpatterns forchaetodontid lin-eages using the pruned time-calibrated phylogeny analyzed with
emspensp emsp | emsp10995DIBATTISTA eT Al
theRpackageBioGeoBEARS(Matzke2013)whichallowsseveralmodels of biogeographic evolution to be compared via likelihoodinference and the ability to incorporate a parameter allowing forfounder-eventspeciationFortheseanalyseswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareasGulfofAqabarestoftheRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPOThediscretecodingofgeographicareasadjacenttotheArabianPeninsulaenablesafine-scaleinvestigationoftheances-tralbiogeographyofthatregionforourtaxaofinterestPresenceabsenceandgeographicalrangedataforeachtaxonwereobtainedfromacombinationofDiBattistaRobertsetal(2016)andFishBase(FroeseampPauly2011)Prognathodesspp(aChaetodontidaegenus)werenotconsideredinthispartoftheanalysisgiventhatthesetwotaxaarerestrictedtotropicalAtlanticwaters
Weconstrainedourbiogeographicanalysestoprohibitcoloniza-tioneventsbetweentheRedSeaandIndianPOregionsbefore5Mareflectingthetimewhenamorepermanentconnectionwasformedvia theStraitofBabalMandab (Bailey2010)OurBioGeoBEARSanalysis evaluated the DEC DIVALIKE and BAYAREALIKE mod-elswithandwithoutthejump(J)parameter(Matzke2013)Thesemodels describe biogeographic scenarios where dispersal extinc-tioncladogenesisvicarianceandfoundereventsaredifferentiallyinvokedtoexplainpresentdaydistributionalpatterns Inourcasewewereinterestedinwhethertherange-restrictedendemicsfromthecoastalwatersoftheArabianPeninsularepresentancientrelictsnew colonization events andor a sourceof biodiversity (at somepointinthepast)forthebroaderIndo-WestPacific
27emsp|emspComparative trait analysis evaluation of the ldquoecological traitrdquo hypothesis
In order to determine whether particular species-level traitswere associatedwith the evolutionof endemism in this subset ofChaetodontidaespecieswefittedaphylogeneticgeneralizedlinearmodel(functionldquophyloglmrdquoinRpackageldquophylolmrdquo[Hoetal2016])thatassumedldquoregionalendemismrdquo(ieendemictothecoastalwa-tersoftheArabianPeninsulaDiBattistaRobertsetal2016)asthebinomialresponsevariableandasuiteofecologicaltraitsasthepre-dictivefixedfactorsFormodelselectionweperformedabackwardstepwiseprocedureforPGLMrsquos(functionldquophylosteprdquoinRpackageldquophylolmrdquo[Hoetal2016])whichentailedsequentialoptimizationbyremovingnon-influentialfixed-effecttermsfromthefullmodelbasedonAkaikeinformationcriteria(AIC)Fulldetailsonthemeth-odsanddatasourcesareprovidedinSupportingInformationTableS2Wealsoexplore interactionsamongthepredictivetraitsusinga regression tree approach (Dersquoath and Fabricius 2000 functionldquorpartrdquoinRpackageldquorpartrdquo[Therneauetal2015])
Amongthepredictivevariablesconsideredweremaximumbodysize(totallength=TLAllenetal1998Kuiter2002)depthrangeinhabited (Allenet al1998) social structure (threecategoriesor-deredfromlowtohighsociabilitysolitarypairformationandgroupformation Allen et al 1998 Kuiter 2002 Yabuta and Berumen
2013) habitat breadth (estimated as the sum value of all habitattypes inhabited C=coral R=rocky D=deep reef S=sedimentR=rubbleCO=coastalCA=algalbedsAllenetal1998Kuiter2002)anddietaryrelianceoncoral reefs (fourcategoriesorderedfromlowtohighrelianceplanktivorebenthicinvertivorefaculta-tivecorallivoreandobligatecorallivoreColeandPratchett2014)Wealsoincludedthephylogeneticageofspecies(Myr)asanaddi-tional fixedfactor totestwhetherspecies traitsare influencedbytimeofdivergencefromsistertaxaForphylogeneticageweeval-uate for each species (regional endemic andwidespread)whetherwe sampled its closest sister speciesby comparingourphylogenywith those published previously (CowmanampBellwood 2011) andotherpublishedaccounts(Kuiter2002)Theecologicaltraitswereselected because they are associated with specialization fitnessandrangeexpansioninbutterflyfishesandthusmayhelptoexplainpatternsofevolutioninfishendemictothecoralreefsoftheArabianPeninsulaWedonotethismaybeanoversimplificationgiventhatourcategoriesarecoarseandbiasedtowardadultversuslarvaltraitswhichare themselvesdatadeficientPreviousworkhoweverhasdemonstratedthattraitsassociatedwiththesuccessfulrecruitmentofreeffisharemoreimportantthantraitsassociatedwithdispersalindeterminingdifferentiationbetweenhabitats(Gaitheretal2015KeithWoolseyMadinByrneampBaird2015)
3emsp |emspRESULTS
31emsp|emspUCE sequences
ReadscontigsandUCElociperindividualareoutlinedinSupportingInformationTableS3Insummarywesequencedatotalof15331millionreadswithameanof155millionreadspersamplefrom47focaltaxa(excludingoutgroupsalsoseeTable1)Overallweassem-bledameanof12969contigs(95CImin=10593max=15345)and901UCElocipersample(95CImin=871max=932)
32emsp|emspPhylogenetic reconstruction and timing of divergence evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Followingassemblyalignmenttrimmingandfilteringoutlocithatwerepresentinfewerthan75specimens(fora75completedata-set)we retained971 alignmentswith amean length of 5156bpThe concatenated supermatrix contained500642bpwith52680informativesitesandwas833completebasedontheproportionofnon-gapsequencesThefollowingsampleswereexcludedfromfurtheranalysisduetothelownumberoflocirecoveredChaetodon_interruptus1a Chaetodon_lineolatus1a Chaetodon_lunula1a andChaetodon ulietensis1a (for full details see Supporting InformationTableS1) however tissue replicateswere retained for twoof thefourspecieslistedhere(Chaetodon lineolatusandChaetodon lunula)
Our Bayesian and maximum likelihood analyses produced afully resolvedtopologythatsharedkeypointsofcongruencewithpriormulti-locus studies of butterflyfishes (Bellwood et al 2010
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
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HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
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RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
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RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
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SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
10990emsp |emsp emspensp DIBATTISTA eT Al
1emsp |emspINTRODUC TION
Explaining the underlying factors responsible for the diversity ofspecies accumulated at hotspots of endemism remains a difficultprobleminthefieldofbiogeographyRecentresearchhasidentifiedtheimportanceofperipheralregionsfromtropicaloceansingener-atingandexportingbiologicaldiversitythusintermittentlyseedingadjacent seas (BowenRocha ToonenampKarl 2013DiBattista etal2013DiBattistaWilcoxCraigRochaampBowen2010Ebleetal2011Gaitheretal2011GaitherToonenRobertsonPlanesampBowen2010MalayampPaulay2010SkillingsBirdampToonen2010)howeverdirecttestsofthisassumptionarerareRenewedinterestin theRedSea toArabianGulf (orPersianGulf) regionprovidesanew opportunity to explore hypotheses associated with how en-demicsareformedinperipheralareasanditspotentialcontributiontothespeciesrichnessofmarinebiodiversityhotspotsTheRedSeaisasemi-enclosedbasinlocatedatthenorth-westerncorneroftheIndianOceanandharborsoneofthehighestlevelsofendemismformarineorganisms(129forfishes126forpolychaetes81forechinoderms 165 for ascidians and 58 for scleractinian cor-alsDiBattistaRobertsetal2016)Thelevelofendemismamongwell-characterizedgroupsintheRedSeasuchastheshorefishesexceedsthoseofallotherperipheralendemichotspotsidentifiedfortheIndianOcean(DiBattistaRobertsetal2016)AlthoughmanyoftheseRedSeaendemicsextendtheirdistribution intotheadja-centGulfofAdenandArabianSea(DiBattistaChoatetal2016DiBattistaRobertsetal2016Kemp1998)itisnotclearwhethertheyarepaleo-endemics(oldlineagesrestrictedduetorangecon-traction) neo-endemics (young lineages at the site of origin) orldquoecologicalrdquoendemics(oldoryounglineageswitharestrictedrangeduetospeciesecologyseeCowmanParraviciniKulbickiampFloeter2017)andwherewhenandhowthisdiversificationoccurred
TheRedSeahasauniquegeologicalandpaleoclimatichistorythatmayhaveplayedaroleinitshighlevelsofendemism(seeDiBattistaChoatetal2016forreview)InbrieftheRedSeabasinwasformedbyepisodesofseafloorspreading41ndash34Ma(GirdlerampStyles1974)followedby intermittentconnections to theMediterraneanSea inthe north (~14ndash5MaHubert-Ferrari et al 2003) and amore re-centconnectiontotheGulfofAdeninthesouththroughtheStraitofBabalMandab (~5Ma topresentBailey2010)TheStrait isanarrowchannel (29km)withashallowsill (137m)thatconstitutesthe only connection between the Red Sea and the Indian Ocean
(Bailey2010)Waterexchange is regulatedby IndianOceanmon-soonpatterns(RaitsosPradhanBrewinStenchikovampHoteit2013Smeed1997)butwashistoricallyminimalorabsentduringreducedsealevelscausedbyglacialperiodsofthePleistocene(Rohlingetal2009)includingthemostrecentglacialmaximum(20ndash15kaLudtampRocha2015Siddalletal2003)RestrictedwaterflowresultedinincreasedsalinitywithintheRedSea(BitonGildorampPeltier2008)leadingsometosuggestthattherewascompleteextirpationofRedSeafaunaduringtheseperiods(Klausewitz1989)TheldquoPleistoceneextirpationrdquohypothesiswhereinallRedSeafaunawereeliminatedduringthe lastglacialmaximum(~18ka)andsubsequentlyre-pop-ulated via more recent colonization events remains controversialand untested with modern comparative approaches (DiBattistaChoatetal2016)althoughsimilargeologicaleventsmayhaveoc-curredintheMediterraneanSea(Bianchietal2012)Thusdespitesomeagreementonthebroadstrokesof itsgeologichistory littleconsensushasemergedontheprocessesthatshapedtheArabianPeninsularsquospresentdaymarinebiodiversitytheirinfluenceonbiodi-versityinadjacentregionsandtheroleofhistoricalclosuresoftheStraitofBabalMandab
ButterflyfishesandbannerfishesbrightlycoloredreeffishesinthefamilyChaetodontidaeareapotentialmodelsystemforeluci-datingtheoriginsmaintenanceandevolutionaryhistoryofRedSeaendemicsandtheirinfluenceonspeciesrichnessinadjacentmarineregionsThefamily isdiverse (17species intheRedSeaandgt130species in the greater Indo-West Pacific Allen Steene amp Allen1998)andphylogeneticallywellresolvedcomparedtootherreeffishfamilies(Cowman2014)AhighproportionoftheChaetodontidaespecies found in the coastal waters of the Arabian Peninsula areendemic (32 DiBattista Roberts et al 2016) Although recentmolecularphylogeniesofchaetodontidshavehelpedtoclarifymanyaspectsoftheirevolutionaryhistory(Bellwoodetal2010Cowmanamp Bellwood 2011 2013 Fessler amp Westneat 2007 HodgeHerwerdenampBellwood2014HsuChenampShao2007)alackofsamplingofArabianPeninsulaspecieshasimpededourunderstand-ingofthediversificationinthisregion
Theevolutionofendemicspecieshasbeenlinkedtoecologicaltraits such as reductions indispersal ability and changes inbodysize(ietheislandrulereviewedbyLomolino2005WhittakerandFernaacutendez-Palacios2007)Forreeffishescertaintraitsassociatedwith dispersal ability are linked to geographic range size For ex-amplelargegregariousandnocturnalspeciestendtohavelarger
drasticallyreducedduringtheextremelowsealevelstandsofglacialagesshallowreefspersistedandassuchtherewasnoevidencesupportingmassextirpationoffaunainthisregion
K E Y W O R D S
biogeographicbarriersChaetodoncoralreefglaciationeventsPleistoceneultraconservedelements
emspensp emsp | emsp10991DIBATTISTA eT Al
rangesizesthansmallsolitaryandstrictlydiurnalspecies(Luizetal20132012)Moreoverdispersalabilitycanpotentiallyinfluencecladediversificationtosuccessfullycolonizeandestablishpopula-tionsinperipheralareastropicalfishspeciesmustbegooddispers-ers(HobbsJonesMundayConnollyampSrinivasan2012)Followingdiversification in peripheral areas newly formed lineages mayevolvetraitslessconducivetodispersalthusbecomingendemictotheareawhereitoriginatedasoftenoccursintheevolutionofinsu-larterrestrialendemics(WhittakerandFernaacutendez-Palacios2007)We thereforepredict thatbutterflyfishesendemic to theArabianPeninsularegionwillhavesmallerbodysizeshighersociabilityandreduceddispersalabilitycomparedtotheirwidespreadcongenersBroadly speaking endemic species tend to be ecological special-istsandthusadaptedtotheenvironmentalconditioninwhichtheyarose (McKinney 1997) We therefore additionally predict thattheseendemicswillhaveahigherlevelofecologicalspecializationthanwidespread species For reef fishes habitat specialization isoftendefinedbythedepthrangewheretheyoccurandthenumberofdifferenthabitatsthattheyexploit(egcoralreefsrockyreefsseagrassbedsmangrovesLuizetal2012)Dietaryspecializationisoftendefinedbytheproportionofdifferentfoodcategoriestar-geted (Pratchett 2014)We predict that butterflyfishes endemictotheArabianPeninsularegionwillhavehigherdietaryspecializa-tionandrelianceoncorals forfoodgivenrecentoriginsalongsidetheircoralrichhabitat(Renemaetal2016)Wechoosetofocusonadultversuslarvalecologicaltraitsbecausemoreinformationabouttheformerisavailableandhasbeenshowntocorrelatewithpast(Ottimofioreetal2017)andpresent(Luizetal2013)geographicrangesize
TheaimsofthisstudyarethreefoldFirstweaimtoreconstructthe phylogeny and evolutionary timescale for Red Sea toArabianGulfbutterflyfishesinordertotestwhethertheseperipheralareasintermittentlyseedthebroaderIndo-WestPacificwithbiodiversity(ldquoevolutionary incubatorrdquo hypothesis)Outcomes thatwould allowrejection of this hypothesis include a lack of evidence supportingArabianPeninsular endemic fish lineages giving rise to Indo-WestPacific fish lineagesaswell as restrictedancestral rangesexpand-ing intothisbroaderregionSecondwe looktotesttheextenttowhich butterflyfishmaintained a continuous presence in the RedSeaduringthemajorenvironmentalfluctuationsofthePleistocene(ldquoPleistoceneextirpationrdquohypothesis)Outcomes thatwould allowrejection of this hypothesis include a lack of evidence supportingArabianPeninsularendemicfishoriginatingaftertheglacialcyclesofthePleistoceneaswellascolonizationeventsdatedonlybeforeorafterthisepochThirdweaimtotestwhetherspeciesendemictothecoastalwatersoftheArabianPeninsulanon-randomlyasso-ciatewithparticularecologicaltraits(ldquoecologicaltraitrdquohypothesis)whichmaybeimportantinexplainingpatternsofdiversificationinthis regionTheexpectationhere is that endemic fishes aremorespecialized and thus better adapted to local conditions than theirwidespreadcongenersOutcomesthatwouldallowrejectionofthishypothesisincludealackofassociationbetweenendemismandanyoftheecologicaltraitsconsideredhere
2emsp |emspMATERIAL S AND METHODS
21emsp|emspMaterials
Site location sampling date and museum voucher information(where available) for each specimen are outlined in SupportingInformationTableS1AllbutterflyfishspeciesincludedinthisstudyandtheirgeographicdistributionarelistedinTable1
Asourprimaryobjectiveistoreconstructtheevolutionaryhis-toryofbutterflyfishesknowntooccurintheRedSeaandadjacentgulfsorseasweconcentratedoursamplingeffortsonthosespe-ciesandtheirclosestrelativesAlthoughfivemajorChaetodontidaelineages were sampled Chaetodon Clade CH1 (Chaetodon robus‐tus andC hoefleri restrictedtotheAtlanticCowmanampBellwood2013) andmultiple bannerfish genera (Amphichaetodon Chelmon Chelmonops Coradion Hemitaurichthys and Johnrandallia) withoutspeciesrepresentedintheRedSeawerenotsampledinthisstudyTwospeciesof thePrognathodes genuswere included to facilitatefossilcalibrationbutwerenotincludedinthebiogeographicanaly-sesduetotheirAtlanticdistributions(seebelow)
Intotalwesampled47chaetodontidspecies(35oftheentirefamily)whichincludesallregionalendemicsandwide-rangingspe-ciesfoundintheArabianPeninsularegionsaveRoa jayakariararedeepwaterspeciesdistributedfromtheRedSeatocoastalIndiawewereunable to secure a tissue sample aspartof this studyEightofthesespecieshavenotpreviouslybeensampledinphylogeneticstudiesof the family (Bellwoodetal2010CowmanampBellwood2011FesslerampWestneat2007Hodgeetal2014)Tissueswerepreservedinasaturatedsalt-DMSOsolutionor95ethanolpriortoprocessingThisresearchwascarriedoutunderthegeneralauspicesofKingAbdullahUniversityofScienceandTechnologyrsquos (KAUST)arrangements for marine research with the Saudi Arabian CoastGuard and the Presidency ofMeteorology and Environment TheanimaluseprotocolwasapprovedbyKAUSTrsquosBiosafetyandEthicsCommittee(KAUSTdoesnotprovidespecificapprovalnumber)
22emsp|emspPhylogenomics approach
We employ the sequence capture method of ultraconserved ele-ments(UCEs)toproducemillionsofreadsinparallelfrommultiplebutterflyfishspecimenscollectedfromtheGulfofAqabainthewest(Red Sea) to theHawaiianArchipelago in the east (PacificOceanPO) UCEs are a class of highly conserved and abundant nuclearmarkers distributed throughout the genomes of most organisms(BejeranoHausslerampBlanchette2004Siepeletal2005Renekeretal2012)Thesemarkersdonotintersectparalogousgenes(DertiRothChurchampWu 2006) do not have retro-element insertions(SimonsPheasantMakuninampMattick2006)havearangeofvari-antsites(ieevolvingondifferenttimescalesFairclothetal2012)andhavebeenusedtoreconstructphylogeniesacrossvertebrates(Bejerano et al 2004 Faircloth et al 2012 Faircloth SorensonSantiniampAlfaro2013McCormacketal2013Smithetal2014Sunetal2014)includingfishesatbothshallow(Mcgeeetal2016)
10992emsp |emsp emspensp DIBATTISTA eT Al
TAB
LE 1
emspSpeciesdistributionandcladedesignationfromBellwoodetal(2010)andCowmanandBellwood(2011)forallChaetodontidaesamplesusedinthisstudy
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Clade4
Chae
todo
n au
riga
radicradic
radicradic
radicradic
radicradic
Chae
todo
n au
ripes
radic
Chae
todo
n co
llare
radicradic
radicradic
radicradic
Chae
todo
n de
cuss
atus
radicradic
Chae
todo
n di
aleu
cos
radicradic
Chae
todo
n fa
lcul
aradic
Chae
todo
n fa
scia
tus
radicradic
radic
Chae
todo
n ga
rdin
eri
radicradic
radicradic
radic
Chae
todo
n le
ucop
leur
aradic
radicradic
radicradic
Chae
todo
n lin
eola
tus
radicradic
radicradic
radicradic
Chae
todo
n lu
nula
radicradic
radicradic
radic
Chae
todo
n m
elan
notu
sradic
radicradic
radicradic
radic
Chae
todo
n m
esol
euco
sradic
radicradic
radic
Chae
todo
n ni
grop
unct
atus
radic
radicradic
Chae
todo
n ox
ycep
halu
sradic
radic
Chae
todo
n pi
ctus
radic
radicradic
radicradic
Chae
todo
n se
mila
rvat
us
radicradic
radicradic
Chae
todo
n va
gabu
ndus
radicradic
radic
Clade3
Chae
todo
n au
stria
cus
radicradic
radicradic
Chae
todo
n ba
rone
ssa
radic
Chae
todo
n be
nnet
tiradic
radicradic
Chae
todo
n la
rvat
us
radicradic
radicradic
Chae
todo
n lu
nula
tus
radic
Chae
todo
n m
elap
teru
sradic
radicradic
radicradic
radic
Chae
todo
n pl
ebei
usradic
Chae
todo
n sp
ecul
umradic
radic
Chae
todo
n tr
iang
ulum
radic
Chae
todo
n tr
ifasc
ialis
radicradic
radicradic
radicradic
radic
Chae
todo
n tr
ifasc
iatu
sradic
radicradic
(Con
tinue
s)
emspensp emsp | emsp10993DIBATTISTA eT Al
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Chae
todo
n za
nzib
arie
nsis
radicradic
radic
Clade2
Chae
todo
n gu
ttat
issim
usradic
radic
Chae
todo
n in
terr
uptu
sradic
Chae
todo
n kl
eini
iradic
radicradic
Chae
todo
n m
adag
aska
riens
isradic
Chae
todo
n m
erte
nsii
radic
Chae
todo
n pa
ucifa
scia
tus
radicradic
radic
Chae
todo
n pe
lew
ensis
radic
Chae
todo
n pu
ncta
tofa
scia
tus
radicradic
Chae
todo
n tr
ichr
ous
radic
Chae
todo
n un
imac
ulat
usradic
radic
Chae
todo
n xa
nthu
rus
radic
Bannerfishes
Forc
ipig
er fl
aviss
imus
radicradic
radicradic
radic
Forc
ipig
er lo
ngiro
stris
radicradic
radic
Hen
ioch
us a
cum
inat
usradic
radicradic
radicradic
radicradic
Hen
ioch
us d
iphr
eute
sradic
radicradic
radicradic
radic
Hen
ioch
us in
term
ediu
sradic
radicradic
ColorsinthetableheadermatchthecolorsusedtodenotespeciesdistributionsinFigure1AsterisksindicateregionalendemicsforthepurposesofourcorrelationaltraitanalysisThelettersbeloweach
regionindicatethegeographicgroupingsusedforBioGeoBEARSanalysisAlthoughC
haet
odon
leuc
ople
uraC
haet
odon
mel
aptu
rusand
Chae
todo
n pi
ctusarelistedasbeingpresentintheRedSeathisis
basedonrarerecordsattheirnorthernlimitsSimilarlywehaveonlysampledC
pic
tus(andnotC
haet
odon
vag
abun
dus)atSocotra(DiBattistaetal2017)andrarerecordsofC
haet
odon
aus
tria
cusinthe
GulfofAdenandSouthOmanlikelyrepresentwaifs
TAB
LE 1
emsp(Continued)
10994emsp |emsp emspensp DIBATTISTA eT Al
anddeep(Alfaroetal2018Fairclothetal2013Harringtonetal2016)phylogeneticscales
23emsp|emspDNA library preparation and next‐generation sequencing
DNA was extracted with DNeasy Blood and Tissue kits (QiagenValenciaCA)whichincludedanRNAseAtreatmentstepEachex-tractedsamplewasvisualizedbygelelectrophoresistoassessDNAqualityTotalDNAfromeachextractedaliquotwasquantifiedusingaQubitdsDNAHSAssayKit(InvitrogenCarlsbadCA)and12microgofDNAperindividualsamplewasfragmentedbysonicationto500basepairs (bp)usingaCovarisS2 sonicator (Covaris IncWoburnMA)andusedforUCElibrarypreparationInbriefweend-repairedadenylated and ligated fragmentedDNA to Illumina TruSeq-styleadapters which included custom sequence tags to barcode eachindividualsample (FairclothampGlenn2012)Followingan18-cyclePCRtoamplify indexed libraries forenrichmentwecreatedpoolsbycombining625ngofeightindividuallibrariesEachpoolwascon-centratedto147ngμlusingavacuumcentrifugeWethenfollowedanestablishedworkflowfortargetenrichment(Gnirkeetal2009)withmodificationsspecifiedinFairclothetal(2012)SpecificallyweenrichedeachpooltargetingUCElociandtheirflankingsequenceusingsyntheticRNAcaptureprobes(MyBaitsMycroarrayIncAnnArborMI)We combined the enriched indexed pools at equimo-lar ratios prior to sequencing The two final pooled librarieswereeach runpaired-end (150bpsequencing)on independent lanesofanIlluminaHiSeq2000(v3reagents)attheKAUSTBioscienceCoreLabDetailedmethodsoflibraryenrichmentpost-enrichmentPCRandvalidationusingrelativeqPCRmaybefoundathttpsultracon-servedorgprotocols
24emsp|emspSequence read quality control assembly and UCE identification
Weremovedadaptercontaminationand lowqualitybaseswith il-lumiprocessor (Faircloth2013)aparallelwrappertoTrimmomatic(BolgerLohseampUsadel2014)ToassemblethetrimmeddatasetweusedthePHYLUCEpipeline (version8ca5884Faircloth2016)with the phyluce_assembly_assemblo_trinitypywrapper script forTrinity(version150Grabherretal2011)WematchedassembledcontigstoenrichedUCElocibyaligningcontigsfromeachspeciesto our UCE probes using the phyluce_assembly_match_contigs_to_probespy scriptwith the LASTZ assembler (Harris 2007)WestoredthesematchresultsintoaSQLiterelationaldatabaseafterex-cludingcontigsthatmatchedmultipleUCElociandUCElociwhoseprobesmatchedmultiplecontigs
Weusedphyluce_align_seqcappytoalignUCElociwithMAFFT(Katohamp Standley 2013KatohMisawaKumaampMiyata 2002)Following alignment we end- and internally-trimmed alignmentswithGBLOCKS (Castresana 2000) to improvephylogenetic infer-encebyremovingpoorlyalignedorhighlydivergentsites(TalaveraampCastresana2007)Weselectedlocithatwerepresentinatleast
75 of our specimens and concatenated the alignments into aPHYLIP-formatted matrix for phylogenetic analysis We includedpreviouslypublishedUCEdataforthreespeciesinouralignmenttorepresentAcanthomorpha outgroup lineages andmore accuratelycalibratethephylogeny(seebelow)
25emsp|emspPhylogenetic analysis of concatenated UCE data evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
WefullypartitionedourconcatenatedalignmentbyUCElocusandperformedBayesiananalysesofthedatasetwithExaBayes(AbererKobert amp Stamatakis 2014) and two independent runs samplingevery500generationsWeusedtheautostoppingconvergencecri-teriaof anaverage standarddeviationof split frequenciesoflt5and visualized the log-likelihood of each chain to ensure conver-genceinTracerversion16(Rambautetal2014)
WeestimateddivergencetimesusingMCMCTREEinthePAMLpackage on the Bayesian consensus topologyWe used the likeli-hood approximation approach following the two-step proceduredescribedbyDosReis andYang (2011) by first estimating ameansubstitutionratefortheentirealignmentwithBASEMLunderastrictmolecularclockandthenusingthisestimatetosetthergene_priorinMCMCTREEWeusedasingleunpartitionedalignmentforcom-putationaltractabilitywithanHKY85modelfivecategoriesforthegammadistributionofrateheterogeneityanrgene_gammapriorforthe gamma distribution describing gene rate heterogeneity of (237105751)andasigma2_gammapriorof (251)WeadoptedacalibrationstrategythatbuildsonHarringtonetal(2016)byinclud-ingmoreproximalacanthomorphoutgroupstoChaetodontidaeandtheirimmediaterelativesWeconstrainedsixnodesonthebasisoffossilinformationusinghardlowerandsoftupperboundsoutlinedinSupportingInformationFigureS1Weassignedaminimumamountofpriorweightforagesbelowthelowerbound(1e-200)and5priorweightforageshigherthantheupperboundBrieflywelinkaseriesofcarangimorphsyngnathiformholocentroidandlampridiformfossilstothesequencesofacanthomorphoutgroupfossilsasperHarringtonet al (2016) This resulted in the following outgroup node calibra-tions acanthuroids versus all other taxa (lower bound 5417Maupperbound7084Ma)acanthuridsversuszanclids (lowerbound490Ma upper bound 627Ma) Naso versus Acanthurus (lowerbound 490Ma upper bound 5722Ma) Chaetodontidae versusPomacanthidae (lower bound 2962Ma upper bound 5926Ma)and the total-group Chaetodon versus Prognathodes (lower bound7Maupperbound475Ma)FurtherjustificationforcalibrationsisavailableasSupportingInformation(AppendixS1)
26emsp|emspAncestral biogeographic range estimation evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Weestimatedancestraldistributionpatterns forchaetodontid lin-eages using the pruned time-calibrated phylogeny analyzed with
emspensp emsp | emsp10995DIBATTISTA eT Al
theRpackageBioGeoBEARS(Matzke2013)whichallowsseveralmodels of biogeographic evolution to be compared via likelihoodinference and the ability to incorporate a parameter allowing forfounder-eventspeciationFortheseanalyseswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareasGulfofAqabarestoftheRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPOThediscretecodingofgeographicareasadjacenttotheArabianPeninsulaenablesafine-scaleinvestigationoftheances-tralbiogeographyofthatregionforourtaxaofinterestPresenceabsenceandgeographicalrangedataforeachtaxonwereobtainedfromacombinationofDiBattistaRobertsetal(2016)andFishBase(FroeseampPauly2011)Prognathodesspp(aChaetodontidaegenus)werenotconsideredinthispartoftheanalysisgiventhatthesetwotaxaarerestrictedtotropicalAtlanticwaters
Weconstrainedourbiogeographicanalysestoprohibitcoloniza-tioneventsbetweentheRedSeaandIndianPOregionsbefore5Mareflectingthetimewhenamorepermanentconnectionwasformedvia theStraitofBabalMandab (Bailey2010)OurBioGeoBEARSanalysis evaluated the DEC DIVALIKE and BAYAREALIKE mod-elswithandwithoutthejump(J)parameter(Matzke2013)Thesemodels describe biogeographic scenarios where dispersal extinc-tioncladogenesisvicarianceandfoundereventsaredifferentiallyinvokedtoexplainpresentdaydistributionalpatterns Inourcasewewereinterestedinwhethertherange-restrictedendemicsfromthecoastalwatersoftheArabianPeninsularepresentancientrelictsnew colonization events andor a sourceof biodiversity (at somepointinthepast)forthebroaderIndo-WestPacific
27emsp|emspComparative trait analysis evaluation of the ldquoecological traitrdquo hypothesis
In order to determine whether particular species-level traitswere associatedwith the evolutionof endemism in this subset ofChaetodontidaespecieswefittedaphylogeneticgeneralizedlinearmodel(functionldquophyloglmrdquoinRpackageldquophylolmrdquo[Hoetal2016])thatassumedldquoregionalendemismrdquo(ieendemictothecoastalwa-tersoftheArabianPeninsulaDiBattistaRobertsetal2016)asthebinomialresponsevariableandasuiteofecologicaltraitsasthepre-dictivefixedfactorsFormodelselectionweperformedabackwardstepwiseprocedureforPGLMrsquos(functionldquophylosteprdquoinRpackageldquophylolmrdquo[Hoetal2016])whichentailedsequentialoptimizationbyremovingnon-influentialfixed-effecttermsfromthefullmodelbasedonAkaikeinformationcriteria(AIC)Fulldetailsonthemeth-odsanddatasourcesareprovidedinSupportingInformationTableS2Wealsoexplore interactionsamongthepredictivetraitsusinga regression tree approach (Dersquoath and Fabricius 2000 functionldquorpartrdquoinRpackageldquorpartrdquo[Therneauetal2015])
Amongthepredictivevariablesconsideredweremaximumbodysize(totallength=TLAllenetal1998Kuiter2002)depthrangeinhabited (Allenet al1998) social structure (threecategoriesor-deredfromlowtohighsociabilitysolitarypairformationandgroupformation Allen et al 1998 Kuiter 2002 Yabuta and Berumen
2013) habitat breadth (estimated as the sum value of all habitattypes inhabited C=coral R=rocky D=deep reef S=sedimentR=rubbleCO=coastalCA=algalbedsAllenetal1998Kuiter2002)anddietaryrelianceoncoral reefs (fourcategoriesorderedfromlowtohighrelianceplanktivorebenthicinvertivorefaculta-tivecorallivoreandobligatecorallivoreColeandPratchett2014)Wealsoincludedthephylogeneticageofspecies(Myr)asanaddi-tional fixedfactor totestwhetherspecies traitsare influencedbytimeofdivergencefromsistertaxaForphylogeneticageweeval-uate for each species (regional endemic andwidespread)whetherwe sampled its closest sister speciesby comparingourphylogenywith those published previously (CowmanampBellwood 2011) andotherpublishedaccounts(Kuiter2002)Theecologicaltraitswereselected because they are associated with specialization fitnessandrangeexpansioninbutterflyfishesandthusmayhelptoexplainpatternsofevolutioninfishendemictothecoralreefsoftheArabianPeninsulaWedonotethismaybeanoversimplificationgiventhatourcategoriesarecoarseandbiasedtowardadultversuslarvaltraitswhichare themselvesdatadeficientPreviousworkhoweverhasdemonstratedthattraitsassociatedwiththesuccessfulrecruitmentofreeffisharemoreimportantthantraitsassociatedwithdispersalindeterminingdifferentiationbetweenhabitats(Gaitheretal2015KeithWoolseyMadinByrneampBaird2015)
3emsp |emspRESULTS
31emsp|emspUCE sequences
ReadscontigsandUCElociperindividualareoutlinedinSupportingInformationTableS3Insummarywesequencedatotalof15331millionreadswithameanof155millionreadspersamplefrom47focaltaxa(excludingoutgroupsalsoseeTable1)Overallweassem-bledameanof12969contigs(95CImin=10593max=15345)and901UCElocipersample(95CImin=871max=932)
32emsp|emspPhylogenetic reconstruction and timing of divergence evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Followingassemblyalignmenttrimmingandfilteringoutlocithatwerepresentinfewerthan75specimens(fora75completedata-set)we retained971 alignmentswith amean length of 5156bpThe concatenated supermatrix contained500642bpwith52680informativesitesandwas833completebasedontheproportionofnon-gapsequencesThefollowingsampleswereexcludedfromfurtheranalysisduetothelownumberoflocirecoveredChaetodon_interruptus1a Chaetodon_lineolatus1a Chaetodon_lunula1a andChaetodon ulietensis1a (for full details see Supporting InformationTableS1) however tissue replicateswere retained for twoof thefourspecieslistedhere(Chaetodon lineolatusandChaetodon lunula)
Our Bayesian and maximum likelihood analyses produced afully resolvedtopologythatsharedkeypointsofcongruencewithpriormulti-locus studies of butterflyfishes (Bellwood et al 2010
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
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AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp10991DIBATTISTA eT Al
rangesizesthansmallsolitaryandstrictlydiurnalspecies(Luizetal20132012)Moreoverdispersalabilitycanpotentiallyinfluencecladediversificationtosuccessfullycolonizeandestablishpopula-tionsinperipheralareastropicalfishspeciesmustbegooddispers-ers(HobbsJonesMundayConnollyampSrinivasan2012)Followingdiversification in peripheral areas newly formed lineages mayevolvetraitslessconducivetodispersalthusbecomingendemictotheareawhereitoriginatedasoftenoccursintheevolutionofinsu-larterrestrialendemics(WhittakerandFernaacutendez-Palacios2007)We thereforepredict thatbutterflyfishesendemic to theArabianPeninsularegionwillhavesmallerbodysizeshighersociabilityandreduceddispersalabilitycomparedtotheirwidespreadcongenersBroadly speaking endemic species tend to be ecological special-istsandthusadaptedtotheenvironmentalconditioninwhichtheyarose (McKinney 1997) We therefore additionally predict thattheseendemicswillhaveahigherlevelofecologicalspecializationthanwidespread species For reef fishes habitat specialization isoftendefinedbythedepthrangewheretheyoccurandthenumberofdifferenthabitatsthattheyexploit(egcoralreefsrockyreefsseagrassbedsmangrovesLuizetal2012)Dietaryspecializationisoftendefinedbytheproportionofdifferentfoodcategoriestar-geted (Pratchett 2014)We predict that butterflyfishes endemictotheArabianPeninsularegionwillhavehigherdietaryspecializa-tionandrelianceoncorals forfoodgivenrecentoriginsalongsidetheircoralrichhabitat(Renemaetal2016)Wechoosetofocusonadultversuslarvalecologicaltraitsbecausemoreinformationabouttheformerisavailableandhasbeenshowntocorrelatewithpast(Ottimofioreetal2017)andpresent(Luizetal2013)geographicrangesize
TheaimsofthisstudyarethreefoldFirstweaimtoreconstructthe phylogeny and evolutionary timescale for Red Sea toArabianGulfbutterflyfishesinordertotestwhethertheseperipheralareasintermittentlyseedthebroaderIndo-WestPacificwithbiodiversity(ldquoevolutionary incubatorrdquo hypothesis)Outcomes thatwould allowrejection of this hypothesis include a lack of evidence supportingArabianPeninsular endemic fish lineages giving rise to Indo-WestPacific fish lineagesaswell as restrictedancestral rangesexpand-ing intothisbroaderregionSecondwe looktotesttheextenttowhich butterflyfishmaintained a continuous presence in the RedSeaduringthemajorenvironmentalfluctuationsofthePleistocene(ldquoPleistoceneextirpationrdquohypothesis)Outcomes thatwould allowrejection of this hypothesis include a lack of evidence supportingArabianPeninsularendemicfishoriginatingaftertheglacialcyclesofthePleistoceneaswellascolonizationeventsdatedonlybeforeorafterthisepochThirdweaimtotestwhetherspeciesendemictothecoastalwatersoftheArabianPeninsulanon-randomlyasso-ciatewithparticularecologicaltraits(ldquoecologicaltraitrdquohypothesis)whichmaybeimportantinexplainingpatternsofdiversificationinthis regionTheexpectationhere is that endemic fishes aremorespecialized and thus better adapted to local conditions than theirwidespreadcongenersOutcomesthatwouldallowrejectionofthishypothesisincludealackofassociationbetweenendemismandanyoftheecologicaltraitsconsideredhere
2emsp |emspMATERIAL S AND METHODS
21emsp|emspMaterials
Site location sampling date and museum voucher information(where available) for each specimen are outlined in SupportingInformationTableS1AllbutterflyfishspeciesincludedinthisstudyandtheirgeographicdistributionarelistedinTable1
Asourprimaryobjectiveistoreconstructtheevolutionaryhis-toryofbutterflyfishesknowntooccurintheRedSeaandadjacentgulfsorseasweconcentratedoursamplingeffortsonthosespe-ciesandtheirclosestrelativesAlthoughfivemajorChaetodontidaelineages were sampled Chaetodon Clade CH1 (Chaetodon robus‐tus andC hoefleri restrictedtotheAtlanticCowmanampBellwood2013) andmultiple bannerfish genera (Amphichaetodon Chelmon Chelmonops Coradion Hemitaurichthys and Johnrandallia) withoutspeciesrepresentedintheRedSeawerenotsampledinthisstudyTwospeciesof thePrognathodes genuswere included to facilitatefossilcalibrationbutwerenotincludedinthebiogeographicanaly-sesduetotheirAtlanticdistributions(seebelow)
Intotalwesampled47chaetodontidspecies(35oftheentirefamily)whichincludesallregionalendemicsandwide-rangingspe-ciesfoundintheArabianPeninsularegionsaveRoa jayakariararedeepwaterspeciesdistributedfromtheRedSeatocoastalIndiawewereunable to secure a tissue sample aspartof this studyEightofthesespecieshavenotpreviouslybeensampledinphylogeneticstudiesof the family (Bellwoodetal2010CowmanampBellwood2011FesslerampWestneat2007Hodgeetal2014)Tissueswerepreservedinasaturatedsalt-DMSOsolutionor95ethanolpriortoprocessingThisresearchwascarriedoutunderthegeneralauspicesofKingAbdullahUniversityofScienceandTechnologyrsquos (KAUST)arrangements for marine research with the Saudi Arabian CoastGuard and the Presidency ofMeteorology and Environment TheanimaluseprotocolwasapprovedbyKAUSTrsquosBiosafetyandEthicsCommittee(KAUSTdoesnotprovidespecificapprovalnumber)
22emsp|emspPhylogenomics approach
We employ the sequence capture method of ultraconserved ele-ments(UCEs)toproducemillionsofreadsinparallelfrommultiplebutterflyfishspecimenscollectedfromtheGulfofAqabainthewest(Red Sea) to theHawaiianArchipelago in the east (PacificOceanPO) UCEs are a class of highly conserved and abundant nuclearmarkers distributed throughout the genomes of most organisms(BejeranoHausslerampBlanchette2004Siepeletal2005Renekeretal2012)Thesemarkersdonotintersectparalogousgenes(DertiRothChurchampWu 2006) do not have retro-element insertions(SimonsPheasantMakuninampMattick2006)havearangeofvari-antsites(ieevolvingondifferenttimescalesFairclothetal2012)andhavebeenusedtoreconstructphylogeniesacrossvertebrates(Bejerano et al 2004 Faircloth et al 2012 Faircloth SorensonSantiniampAlfaro2013McCormacketal2013Smithetal2014Sunetal2014)includingfishesatbothshallow(Mcgeeetal2016)
10992emsp |emsp emspensp DIBATTISTA eT Al
TAB
LE 1
emspSpeciesdistributionandcladedesignationfromBellwoodetal(2010)andCowmanandBellwood(2011)forallChaetodontidaesamplesusedinthisstudy
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Clade4
Chae
todo
n au
riga
radicradic
radicradic
radicradic
radicradic
Chae
todo
n au
ripes
radic
Chae
todo
n co
llare
radicradic
radicradic
radicradic
Chae
todo
n de
cuss
atus
radicradic
Chae
todo
n di
aleu
cos
radicradic
Chae
todo
n fa
lcul
aradic
Chae
todo
n fa
scia
tus
radicradic
radic
Chae
todo
n ga
rdin
eri
radicradic
radicradic
radic
Chae
todo
n le
ucop
leur
aradic
radicradic
radicradic
Chae
todo
n lin
eola
tus
radicradic
radicradic
radicradic
Chae
todo
n lu
nula
radicradic
radicradic
radic
Chae
todo
n m
elan
notu
sradic
radicradic
radicradic
radic
Chae
todo
n m
esol
euco
sradic
radicradic
radic
Chae
todo
n ni
grop
unct
atus
radic
radicradic
Chae
todo
n ox
ycep
halu
sradic
radic
Chae
todo
n pi
ctus
radic
radicradic
radicradic
Chae
todo
n se
mila
rvat
us
radicradic
radicradic
Chae
todo
n va
gabu
ndus
radicradic
radic
Clade3
Chae
todo
n au
stria
cus
radicradic
radicradic
Chae
todo
n ba
rone
ssa
radic
Chae
todo
n be
nnet
tiradic
radicradic
Chae
todo
n la
rvat
us
radicradic
radicradic
Chae
todo
n lu
nula
tus
radic
Chae
todo
n m
elap
teru
sradic
radicradic
radicradic
radic
Chae
todo
n pl
ebei
usradic
Chae
todo
n sp
ecul
umradic
radic
Chae
todo
n tr
iang
ulum
radic
Chae
todo
n tr
ifasc
ialis
radicradic
radicradic
radicradic
radic
Chae
todo
n tr
ifasc
iatu
sradic
radicradic
(Con
tinue
s)
emspensp emsp | emsp10993DIBATTISTA eT Al
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Chae
todo
n za
nzib
arie
nsis
radicradic
radic
Clade2
Chae
todo
n gu
ttat
issim
usradic
radic
Chae
todo
n in
terr
uptu
sradic
Chae
todo
n kl
eini
iradic
radicradic
Chae
todo
n m
adag
aska
riens
isradic
Chae
todo
n m
erte
nsii
radic
Chae
todo
n pa
ucifa
scia
tus
radicradic
radic
Chae
todo
n pe
lew
ensis
radic
Chae
todo
n pu
ncta
tofa
scia
tus
radicradic
Chae
todo
n tr
ichr
ous
radic
Chae
todo
n un
imac
ulat
usradic
radic
Chae
todo
n xa
nthu
rus
radic
Bannerfishes
Forc
ipig
er fl
aviss
imus
radicradic
radicradic
radic
Forc
ipig
er lo
ngiro
stris
radicradic
radic
Hen
ioch
us a
cum
inat
usradic
radicradic
radicradic
radicradic
Hen
ioch
us d
iphr
eute
sradic
radicradic
radicradic
radic
Hen
ioch
us in
term
ediu
sradic
radicradic
ColorsinthetableheadermatchthecolorsusedtodenotespeciesdistributionsinFigure1AsterisksindicateregionalendemicsforthepurposesofourcorrelationaltraitanalysisThelettersbeloweach
regionindicatethegeographicgroupingsusedforBioGeoBEARSanalysisAlthoughC
haet
odon
leuc
ople
uraC
haet
odon
mel
aptu
rusand
Chae
todo
n pi
ctusarelistedasbeingpresentintheRedSeathisis
basedonrarerecordsattheirnorthernlimitsSimilarlywehaveonlysampledC
pic
tus(andnotC
haet
odon
vag
abun
dus)atSocotra(DiBattistaetal2017)andrarerecordsofC
haet
odon
aus
tria
cusinthe
GulfofAdenandSouthOmanlikelyrepresentwaifs
TAB
LE 1
emsp(Continued)
10994emsp |emsp emspensp DIBATTISTA eT Al
anddeep(Alfaroetal2018Fairclothetal2013Harringtonetal2016)phylogeneticscales
23emsp|emspDNA library preparation and next‐generation sequencing
DNA was extracted with DNeasy Blood and Tissue kits (QiagenValenciaCA)whichincludedanRNAseAtreatmentstepEachex-tractedsamplewasvisualizedbygelelectrophoresistoassessDNAqualityTotalDNAfromeachextractedaliquotwasquantifiedusingaQubitdsDNAHSAssayKit(InvitrogenCarlsbadCA)and12microgofDNAperindividualsamplewasfragmentedbysonicationto500basepairs (bp)usingaCovarisS2 sonicator (Covaris IncWoburnMA)andusedforUCElibrarypreparationInbriefweend-repairedadenylated and ligated fragmentedDNA to Illumina TruSeq-styleadapters which included custom sequence tags to barcode eachindividualsample (FairclothampGlenn2012)Followingan18-cyclePCRtoamplify indexed libraries forenrichmentwecreatedpoolsbycombining625ngofeightindividuallibrariesEachpoolwascon-centratedto147ngμlusingavacuumcentrifugeWethenfollowedanestablishedworkflowfortargetenrichment(Gnirkeetal2009)withmodificationsspecifiedinFairclothetal(2012)SpecificallyweenrichedeachpooltargetingUCElociandtheirflankingsequenceusingsyntheticRNAcaptureprobes(MyBaitsMycroarrayIncAnnArborMI)We combined the enriched indexed pools at equimo-lar ratios prior to sequencing The two final pooled librarieswereeach runpaired-end (150bpsequencing)on independent lanesofanIlluminaHiSeq2000(v3reagents)attheKAUSTBioscienceCoreLabDetailedmethodsoflibraryenrichmentpost-enrichmentPCRandvalidationusingrelativeqPCRmaybefoundathttpsultracon-servedorgprotocols
24emsp|emspSequence read quality control assembly and UCE identification
Weremovedadaptercontaminationand lowqualitybaseswith il-lumiprocessor (Faircloth2013)aparallelwrappertoTrimmomatic(BolgerLohseampUsadel2014)ToassemblethetrimmeddatasetweusedthePHYLUCEpipeline (version8ca5884Faircloth2016)with the phyluce_assembly_assemblo_trinitypywrapper script forTrinity(version150Grabherretal2011)WematchedassembledcontigstoenrichedUCElocibyaligningcontigsfromeachspeciesto our UCE probes using the phyluce_assembly_match_contigs_to_probespy scriptwith the LASTZ assembler (Harris 2007)WestoredthesematchresultsintoaSQLiterelationaldatabaseafterex-cludingcontigsthatmatchedmultipleUCElociandUCElociwhoseprobesmatchedmultiplecontigs
Weusedphyluce_align_seqcappytoalignUCElociwithMAFFT(Katohamp Standley 2013KatohMisawaKumaampMiyata 2002)Following alignment we end- and internally-trimmed alignmentswithGBLOCKS (Castresana 2000) to improvephylogenetic infer-encebyremovingpoorlyalignedorhighlydivergentsites(TalaveraampCastresana2007)Weselectedlocithatwerepresentinatleast
75 of our specimens and concatenated the alignments into aPHYLIP-formatted matrix for phylogenetic analysis We includedpreviouslypublishedUCEdataforthreespeciesinouralignmenttorepresentAcanthomorpha outgroup lineages andmore accuratelycalibratethephylogeny(seebelow)
25emsp|emspPhylogenetic analysis of concatenated UCE data evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
WefullypartitionedourconcatenatedalignmentbyUCElocusandperformedBayesiananalysesofthedatasetwithExaBayes(AbererKobert amp Stamatakis 2014) and two independent runs samplingevery500generationsWeusedtheautostoppingconvergencecri-teriaof anaverage standarddeviationof split frequenciesoflt5and visualized the log-likelihood of each chain to ensure conver-genceinTracerversion16(Rambautetal2014)
WeestimateddivergencetimesusingMCMCTREEinthePAMLpackage on the Bayesian consensus topologyWe used the likeli-hood approximation approach following the two-step proceduredescribedbyDosReis andYang (2011) by first estimating ameansubstitutionratefortheentirealignmentwithBASEMLunderastrictmolecularclockandthenusingthisestimatetosetthergene_priorinMCMCTREEWeusedasingleunpartitionedalignmentforcom-putationaltractabilitywithanHKY85modelfivecategoriesforthegammadistributionofrateheterogeneityanrgene_gammapriorforthe gamma distribution describing gene rate heterogeneity of (237105751)andasigma2_gammapriorof (251)WeadoptedacalibrationstrategythatbuildsonHarringtonetal(2016)byinclud-ingmoreproximalacanthomorphoutgroupstoChaetodontidaeandtheirimmediaterelativesWeconstrainedsixnodesonthebasisoffossilinformationusinghardlowerandsoftupperboundsoutlinedinSupportingInformationFigureS1Weassignedaminimumamountofpriorweightforagesbelowthelowerbound(1e-200)and5priorweightforageshigherthantheupperboundBrieflywelinkaseriesofcarangimorphsyngnathiformholocentroidandlampridiformfossilstothesequencesofacanthomorphoutgroupfossilsasperHarringtonet al (2016) This resulted in the following outgroup node calibra-tions acanthuroids versus all other taxa (lower bound 5417Maupperbound7084Ma)acanthuridsversuszanclids (lowerbound490Ma upper bound 627Ma) Naso versus Acanthurus (lowerbound 490Ma upper bound 5722Ma) Chaetodontidae versusPomacanthidae (lower bound 2962Ma upper bound 5926Ma)and the total-group Chaetodon versus Prognathodes (lower bound7Maupperbound475Ma)FurtherjustificationforcalibrationsisavailableasSupportingInformation(AppendixS1)
26emsp|emspAncestral biogeographic range estimation evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Weestimatedancestraldistributionpatterns forchaetodontid lin-eages using the pruned time-calibrated phylogeny analyzed with
emspensp emsp | emsp10995DIBATTISTA eT Al
theRpackageBioGeoBEARS(Matzke2013)whichallowsseveralmodels of biogeographic evolution to be compared via likelihoodinference and the ability to incorporate a parameter allowing forfounder-eventspeciationFortheseanalyseswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareasGulfofAqabarestoftheRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPOThediscretecodingofgeographicareasadjacenttotheArabianPeninsulaenablesafine-scaleinvestigationoftheances-tralbiogeographyofthatregionforourtaxaofinterestPresenceabsenceandgeographicalrangedataforeachtaxonwereobtainedfromacombinationofDiBattistaRobertsetal(2016)andFishBase(FroeseampPauly2011)Prognathodesspp(aChaetodontidaegenus)werenotconsideredinthispartoftheanalysisgiventhatthesetwotaxaarerestrictedtotropicalAtlanticwaters
Weconstrainedourbiogeographicanalysestoprohibitcoloniza-tioneventsbetweentheRedSeaandIndianPOregionsbefore5Mareflectingthetimewhenamorepermanentconnectionwasformedvia theStraitofBabalMandab (Bailey2010)OurBioGeoBEARSanalysis evaluated the DEC DIVALIKE and BAYAREALIKE mod-elswithandwithoutthejump(J)parameter(Matzke2013)Thesemodels describe biogeographic scenarios where dispersal extinc-tioncladogenesisvicarianceandfoundereventsaredifferentiallyinvokedtoexplainpresentdaydistributionalpatterns Inourcasewewereinterestedinwhethertherange-restrictedendemicsfromthecoastalwatersoftheArabianPeninsularepresentancientrelictsnew colonization events andor a sourceof biodiversity (at somepointinthepast)forthebroaderIndo-WestPacific
27emsp|emspComparative trait analysis evaluation of the ldquoecological traitrdquo hypothesis
In order to determine whether particular species-level traitswere associatedwith the evolutionof endemism in this subset ofChaetodontidaespecieswefittedaphylogeneticgeneralizedlinearmodel(functionldquophyloglmrdquoinRpackageldquophylolmrdquo[Hoetal2016])thatassumedldquoregionalendemismrdquo(ieendemictothecoastalwa-tersoftheArabianPeninsulaDiBattistaRobertsetal2016)asthebinomialresponsevariableandasuiteofecologicaltraitsasthepre-dictivefixedfactorsFormodelselectionweperformedabackwardstepwiseprocedureforPGLMrsquos(functionldquophylosteprdquoinRpackageldquophylolmrdquo[Hoetal2016])whichentailedsequentialoptimizationbyremovingnon-influentialfixed-effecttermsfromthefullmodelbasedonAkaikeinformationcriteria(AIC)Fulldetailsonthemeth-odsanddatasourcesareprovidedinSupportingInformationTableS2Wealsoexplore interactionsamongthepredictivetraitsusinga regression tree approach (Dersquoath and Fabricius 2000 functionldquorpartrdquoinRpackageldquorpartrdquo[Therneauetal2015])
Amongthepredictivevariablesconsideredweremaximumbodysize(totallength=TLAllenetal1998Kuiter2002)depthrangeinhabited (Allenet al1998) social structure (threecategoriesor-deredfromlowtohighsociabilitysolitarypairformationandgroupformation Allen et al 1998 Kuiter 2002 Yabuta and Berumen
2013) habitat breadth (estimated as the sum value of all habitattypes inhabited C=coral R=rocky D=deep reef S=sedimentR=rubbleCO=coastalCA=algalbedsAllenetal1998Kuiter2002)anddietaryrelianceoncoral reefs (fourcategoriesorderedfromlowtohighrelianceplanktivorebenthicinvertivorefaculta-tivecorallivoreandobligatecorallivoreColeandPratchett2014)Wealsoincludedthephylogeneticageofspecies(Myr)asanaddi-tional fixedfactor totestwhetherspecies traitsare influencedbytimeofdivergencefromsistertaxaForphylogeneticageweeval-uate for each species (regional endemic andwidespread)whetherwe sampled its closest sister speciesby comparingourphylogenywith those published previously (CowmanampBellwood 2011) andotherpublishedaccounts(Kuiter2002)Theecologicaltraitswereselected because they are associated with specialization fitnessandrangeexpansioninbutterflyfishesandthusmayhelptoexplainpatternsofevolutioninfishendemictothecoralreefsoftheArabianPeninsulaWedonotethismaybeanoversimplificationgiventhatourcategoriesarecoarseandbiasedtowardadultversuslarvaltraitswhichare themselvesdatadeficientPreviousworkhoweverhasdemonstratedthattraitsassociatedwiththesuccessfulrecruitmentofreeffisharemoreimportantthantraitsassociatedwithdispersalindeterminingdifferentiationbetweenhabitats(Gaitheretal2015KeithWoolseyMadinByrneampBaird2015)
3emsp |emspRESULTS
31emsp|emspUCE sequences
ReadscontigsandUCElociperindividualareoutlinedinSupportingInformationTableS3Insummarywesequencedatotalof15331millionreadswithameanof155millionreadspersamplefrom47focaltaxa(excludingoutgroupsalsoseeTable1)Overallweassem-bledameanof12969contigs(95CImin=10593max=15345)and901UCElocipersample(95CImin=871max=932)
32emsp|emspPhylogenetic reconstruction and timing of divergence evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Followingassemblyalignmenttrimmingandfilteringoutlocithatwerepresentinfewerthan75specimens(fora75completedata-set)we retained971 alignmentswith amean length of 5156bpThe concatenated supermatrix contained500642bpwith52680informativesitesandwas833completebasedontheproportionofnon-gapsequencesThefollowingsampleswereexcludedfromfurtheranalysisduetothelownumberoflocirecoveredChaetodon_interruptus1a Chaetodon_lineolatus1a Chaetodon_lunula1a andChaetodon ulietensis1a (for full details see Supporting InformationTableS1) however tissue replicateswere retained for twoof thefourspecieslistedhere(Chaetodon lineolatusandChaetodon lunula)
Our Bayesian and maximum likelihood analyses produced afully resolvedtopologythatsharedkeypointsofcongruencewithpriormulti-locus studies of butterflyfishes (Bellwood et al 2010
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
AbererA JKobertKampStamatakisA (2014)ExaBayesMassivelyparallelBayesiantreeinferenceforthewhole-genomeeraMolecular Biology and Evolution 31 2553ndash2556 httpsdoiorg101093molbevmsu236
AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
10992emsp |emsp emspensp DIBATTISTA eT Al
TAB
LE 1
emspSpeciesdistributionandcladedesignationfromBellwoodetal(2010)andCowmanandBellwood(2011)forallChaetodontidaesamplesusedinthisstudy
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Clade4
Chae
todo
n au
riga
radicradic
radicradic
radicradic
radicradic
Chae
todo
n au
ripes
radic
Chae
todo
n co
llare
radicradic
radicradic
radicradic
Chae
todo
n de
cuss
atus
radicradic
Chae
todo
n di
aleu
cos
radicradic
Chae
todo
n fa
lcul
aradic
Chae
todo
n fa
scia
tus
radicradic
radic
Chae
todo
n ga
rdin
eri
radicradic
radicradic
radic
Chae
todo
n le
ucop
leur
aradic
radicradic
radicradic
Chae
todo
n lin
eola
tus
radicradic
radicradic
radicradic
Chae
todo
n lu
nula
radicradic
radicradic
radic
Chae
todo
n m
elan
notu
sradic
radicradic
radicradic
radic
Chae
todo
n m
esol
euco
sradic
radicradic
radic
Chae
todo
n ni
grop
unct
atus
radic
radicradic
Chae
todo
n ox
ycep
halu
sradic
radic
Chae
todo
n pi
ctus
radic
radicradic
radicradic
Chae
todo
n se
mila
rvat
us
radicradic
radicradic
Chae
todo
n va
gabu
ndus
radicradic
radic
Clade3
Chae
todo
n au
stria
cus
radicradic
radicradic
Chae
todo
n ba
rone
ssa
radic
Chae
todo
n be
nnet
tiradic
radicradic
Chae
todo
n la
rvat
us
radicradic
radicradic
Chae
todo
n lu
nula
tus
radic
Chae
todo
n m
elap
teru
sradic
radicradic
radicradic
radic
Chae
todo
n pl
ebei
usradic
Chae
todo
n sp
ecul
umradic
radic
Chae
todo
n tr
iang
ulum
radic
Chae
todo
n tr
ifasc
ialis
radicradic
radicradic
radicradic
radic
Chae
todo
n tr
ifasc
iatu
sradic
radicradic
(Con
tinue
s)
emspensp emsp | emsp10993DIBATTISTA eT Al
Spec
ies
Geo
grap
hic
dist
ribut
ion
Gul
f of
Aqa
ba (A
)Re
st o
f Red
Se
a (B
)D
jibou
ti an
d G
ulf o
f A
den
(C)
Soco
tra
(D)
Sout
h O
man
(E)
Ara
bian
Gul
f (F)
Gul
f of O
man
and
Pa
kist
an (G
)Re
st o
f Ind
ian
Oce
an (H
)Pa
cific
Oce
an (I
)
Chae
todo
n za
nzib
arie
nsis
radicradic
radic
Clade2
Chae
todo
n gu
ttat
issim
usradic
radic
Chae
todo
n in
terr
uptu
sradic
Chae
todo
n kl
eini
iradic
radicradic
Chae
todo
n m
adag
aska
riens
isradic
Chae
todo
n m
erte
nsii
radic
Chae
todo
n pa
ucifa
scia
tus
radicradic
radic
Chae
todo
n pe
lew
ensis
radic
Chae
todo
n pu
ncta
tofa
scia
tus
radicradic
Chae
todo
n tr
ichr
ous
radic
Chae
todo
n un
imac
ulat
usradic
radic
Chae
todo
n xa
nthu
rus
radic
Bannerfishes
Forc
ipig
er fl
aviss
imus
radicradic
radicradic
radic
Forc
ipig
er lo
ngiro
stris
radicradic
radic
Hen
ioch
us a
cum
inat
usradic
radicradic
radicradic
radicradic
Hen
ioch
us d
iphr
eute
sradic
radicradic
radicradic
radic
Hen
ioch
us in
term
ediu
sradic
radicradic
ColorsinthetableheadermatchthecolorsusedtodenotespeciesdistributionsinFigure1AsterisksindicateregionalendemicsforthepurposesofourcorrelationaltraitanalysisThelettersbeloweach
regionindicatethegeographicgroupingsusedforBioGeoBEARSanalysisAlthoughC
haet
odon
leuc
ople
uraC
haet
odon
mel
aptu
rusand
Chae
todo
n pi
ctusarelistedasbeingpresentintheRedSeathisis
basedonrarerecordsattheirnorthernlimitsSimilarlywehaveonlysampledC
pic
tus(andnotC
haet
odon
vag
abun
dus)atSocotra(DiBattistaetal2017)andrarerecordsofC
haet
odon
aus
tria
cusinthe
GulfofAdenandSouthOmanlikelyrepresentwaifs
TAB
LE 1
emsp(Continued)
10994emsp |emsp emspensp DIBATTISTA eT Al
anddeep(Alfaroetal2018Fairclothetal2013Harringtonetal2016)phylogeneticscales
23emsp|emspDNA library preparation and next‐generation sequencing
DNA was extracted with DNeasy Blood and Tissue kits (QiagenValenciaCA)whichincludedanRNAseAtreatmentstepEachex-tractedsamplewasvisualizedbygelelectrophoresistoassessDNAqualityTotalDNAfromeachextractedaliquotwasquantifiedusingaQubitdsDNAHSAssayKit(InvitrogenCarlsbadCA)and12microgofDNAperindividualsamplewasfragmentedbysonicationto500basepairs (bp)usingaCovarisS2 sonicator (Covaris IncWoburnMA)andusedforUCElibrarypreparationInbriefweend-repairedadenylated and ligated fragmentedDNA to Illumina TruSeq-styleadapters which included custom sequence tags to barcode eachindividualsample (FairclothampGlenn2012)Followingan18-cyclePCRtoamplify indexed libraries forenrichmentwecreatedpoolsbycombining625ngofeightindividuallibrariesEachpoolwascon-centratedto147ngμlusingavacuumcentrifugeWethenfollowedanestablishedworkflowfortargetenrichment(Gnirkeetal2009)withmodificationsspecifiedinFairclothetal(2012)SpecificallyweenrichedeachpooltargetingUCElociandtheirflankingsequenceusingsyntheticRNAcaptureprobes(MyBaitsMycroarrayIncAnnArborMI)We combined the enriched indexed pools at equimo-lar ratios prior to sequencing The two final pooled librarieswereeach runpaired-end (150bpsequencing)on independent lanesofanIlluminaHiSeq2000(v3reagents)attheKAUSTBioscienceCoreLabDetailedmethodsoflibraryenrichmentpost-enrichmentPCRandvalidationusingrelativeqPCRmaybefoundathttpsultracon-servedorgprotocols
24emsp|emspSequence read quality control assembly and UCE identification
Weremovedadaptercontaminationand lowqualitybaseswith il-lumiprocessor (Faircloth2013)aparallelwrappertoTrimmomatic(BolgerLohseampUsadel2014)ToassemblethetrimmeddatasetweusedthePHYLUCEpipeline (version8ca5884Faircloth2016)with the phyluce_assembly_assemblo_trinitypywrapper script forTrinity(version150Grabherretal2011)WematchedassembledcontigstoenrichedUCElocibyaligningcontigsfromeachspeciesto our UCE probes using the phyluce_assembly_match_contigs_to_probespy scriptwith the LASTZ assembler (Harris 2007)WestoredthesematchresultsintoaSQLiterelationaldatabaseafterex-cludingcontigsthatmatchedmultipleUCElociandUCElociwhoseprobesmatchedmultiplecontigs
Weusedphyluce_align_seqcappytoalignUCElociwithMAFFT(Katohamp Standley 2013KatohMisawaKumaampMiyata 2002)Following alignment we end- and internally-trimmed alignmentswithGBLOCKS (Castresana 2000) to improvephylogenetic infer-encebyremovingpoorlyalignedorhighlydivergentsites(TalaveraampCastresana2007)Weselectedlocithatwerepresentinatleast
75 of our specimens and concatenated the alignments into aPHYLIP-formatted matrix for phylogenetic analysis We includedpreviouslypublishedUCEdataforthreespeciesinouralignmenttorepresentAcanthomorpha outgroup lineages andmore accuratelycalibratethephylogeny(seebelow)
25emsp|emspPhylogenetic analysis of concatenated UCE data evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
WefullypartitionedourconcatenatedalignmentbyUCElocusandperformedBayesiananalysesofthedatasetwithExaBayes(AbererKobert amp Stamatakis 2014) and two independent runs samplingevery500generationsWeusedtheautostoppingconvergencecri-teriaof anaverage standarddeviationof split frequenciesoflt5and visualized the log-likelihood of each chain to ensure conver-genceinTracerversion16(Rambautetal2014)
WeestimateddivergencetimesusingMCMCTREEinthePAMLpackage on the Bayesian consensus topologyWe used the likeli-hood approximation approach following the two-step proceduredescribedbyDosReis andYang (2011) by first estimating ameansubstitutionratefortheentirealignmentwithBASEMLunderastrictmolecularclockandthenusingthisestimatetosetthergene_priorinMCMCTREEWeusedasingleunpartitionedalignmentforcom-putationaltractabilitywithanHKY85modelfivecategoriesforthegammadistributionofrateheterogeneityanrgene_gammapriorforthe gamma distribution describing gene rate heterogeneity of (237105751)andasigma2_gammapriorof (251)WeadoptedacalibrationstrategythatbuildsonHarringtonetal(2016)byinclud-ingmoreproximalacanthomorphoutgroupstoChaetodontidaeandtheirimmediaterelativesWeconstrainedsixnodesonthebasisoffossilinformationusinghardlowerandsoftupperboundsoutlinedinSupportingInformationFigureS1Weassignedaminimumamountofpriorweightforagesbelowthelowerbound(1e-200)and5priorweightforageshigherthantheupperboundBrieflywelinkaseriesofcarangimorphsyngnathiformholocentroidandlampridiformfossilstothesequencesofacanthomorphoutgroupfossilsasperHarringtonet al (2016) This resulted in the following outgroup node calibra-tions acanthuroids versus all other taxa (lower bound 5417Maupperbound7084Ma)acanthuridsversuszanclids (lowerbound490Ma upper bound 627Ma) Naso versus Acanthurus (lowerbound 490Ma upper bound 5722Ma) Chaetodontidae versusPomacanthidae (lower bound 2962Ma upper bound 5926Ma)and the total-group Chaetodon versus Prognathodes (lower bound7Maupperbound475Ma)FurtherjustificationforcalibrationsisavailableasSupportingInformation(AppendixS1)
26emsp|emspAncestral biogeographic range estimation evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Weestimatedancestraldistributionpatterns forchaetodontid lin-eages using the pruned time-calibrated phylogeny analyzed with
emspensp emsp | emsp10995DIBATTISTA eT Al
theRpackageBioGeoBEARS(Matzke2013)whichallowsseveralmodels of biogeographic evolution to be compared via likelihoodinference and the ability to incorporate a parameter allowing forfounder-eventspeciationFortheseanalyseswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareasGulfofAqabarestoftheRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPOThediscretecodingofgeographicareasadjacenttotheArabianPeninsulaenablesafine-scaleinvestigationoftheances-tralbiogeographyofthatregionforourtaxaofinterestPresenceabsenceandgeographicalrangedataforeachtaxonwereobtainedfromacombinationofDiBattistaRobertsetal(2016)andFishBase(FroeseampPauly2011)Prognathodesspp(aChaetodontidaegenus)werenotconsideredinthispartoftheanalysisgiventhatthesetwotaxaarerestrictedtotropicalAtlanticwaters
Weconstrainedourbiogeographicanalysestoprohibitcoloniza-tioneventsbetweentheRedSeaandIndianPOregionsbefore5Mareflectingthetimewhenamorepermanentconnectionwasformedvia theStraitofBabalMandab (Bailey2010)OurBioGeoBEARSanalysis evaluated the DEC DIVALIKE and BAYAREALIKE mod-elswithandwithoutthejump(J)parameter(Matzke2013)Thesemodels describe biogeographic scenarios where dispersal extinc-tioncladogenesisvicarianceandfoundereventsaredifferentiallyinvokedtoexplainpresentdaydistributionalpatterns Inourcasewewereinterestedinwhethertherange-restrictedendemicsfromthecoastalwatersoftheArabianPeninsularepresentancientrelictsnew colonization events andor a sourceof biodiversity (at somepointinthepast)forthebroaderIndo-WestPacific
27emsp|emspComparative trait analysis evaluation of the ldquoecological traitrdquo hypothesis
In order to determine whether particular species-level traitswere associatedwith the evolutionof endemism in this subset ofChaetodontidaespecieswefittedaphylogeneticgeneralizedlinearmodel(functionldquophyloglmrdquoinRpackageldquophylolmrdquo[Hoetal2016])thatassumedldquoregionalendemismrdquo(ieendemictothecoastalwa-tersoftheArabianPeninsulaDiBattistaRobertsetal2016)asthebinomialresponsevariableandasuiteofecologicaltraitsasthepre-dictivefixedfactorsFormodelselectionweperformedabackwardstepwiseprocedureforPGLMrsquos(functionldquophylosteprdquoinRpackageldquophylolmrdquo[Hoetal2016])whichentailedsequentialoptimizationbyremovingnon-influentialfixed-effecttermsfromthefullmodelbasedonAkaikeinformationcriteria(AIC)Fulldetailsonthemeth-odsanddatasourcesareprovidedinSupportingInformationTableS2Wealsoexplore interactionsamongthepredictivetraitsusinga regression tree approach (Dersquoath and Fabricius 2000 functionldquorpartrdquoinRpackageldquorpartrdquo[Therneauetal2015])
Amongthepredictivevariablesconsideredweremaximumbodysize(totallength=TLAllenetal1998Kuiter2002)depthrangeinhabited (Allenet al1998) social structure (threecategoriesor-deredfromlowtohighsociabilitysolitarypairformationandgroupformation Allen et al 1998 Kuiter 2002 Yabuta and Berumen
2013) habitat breadth (estimated as the sum value of all habitattypes inhabited C=coral R=rocky D=deep reef S=sedimentR=rubbleCO=coastalCA=algalbedsAllenetal1998Kuiter2002)anddietaryrelianceoncoral reefs (fourcategoriesorderedfromlowtohighrelianceplanktivorebenthicinvertivorefaculta-tivecorallivoreandobligatecorallivoreColeandPratchett2014)Wealsoincludedthephylogeneticageofspecies(Myr)asanaddi-tional fixedfactor totestwhetherspecies traitsare influencedbytimeofdivergencefromsistertaxaForphylogeneticageweeval-uate for each species (regional endemic andwidespread)whetherwe sampled its closest sister speciesby comparingourphylogenywith those published previously (CowmanampBellwood 2011) andotherpublishedaccounts(Kuiter2002)Theecologicaltraitswereselected because they are associated with specialization fitnessandrangeexpansioninbutterflyfishesandthusmayhelptoexplainpatternsofevolutioninfishendemictothecoralreefsoftheArabianPeninsulaWedonotethismaybeanoversimplificationgiventhatourcategoriesarecoarseandbiasedtowardadultversuslarvaltraitswhichare themselvesdatadeficientPreviousworkhoweverhasdemonstratedthattraitsassociatedwiththesuccessfulrecruitmentofreeffisharemoreimportantthantraitsassociatedwithdispersalindeterminingdifferentiationbetweenhabitats(Gaitheretal2015KeithWoolseyMadinByrneampBaird2015)
3emsp |emspRESULTS
31emsp|emspUCE sequences
ReadscontigsandUCElociperindividualareoutlinedinSupportingInformationTableS3Insummarywesequencedatotalof15331millionreadswithameanof155millionreadspersamplefrom47focaltaxa(excludingoutgroupsalsoseeTable1)Overallweassem-bledameanof12969contigs(95CImin=10593max=15345)and901UCElocipersample(95CImin=871max=932)
32emsp|emspPhylogenetic reconstruction and timing of divergence evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Followingassemblyalignmenttrimmingandfilteringoutlocithatwerepresentinfewerthan75specimens(fora75completedata-set)we retained971 alignmentswith amean length of 5156bpThe concatenated supermatrix contained500642bpwith52680informativesitesandwas833completebasedontheproportionofnon-gapsequencesThefollowingsampleswereexcludedfromfurtheranalysisduetothelownumberoflocirecoveredChaetodon_interruptus1a Chaetodon_lineolatus1a Chaetodon_lunula1a andChaetodon ulietensis1a (for full details see Supporting InformationTableS1) however tissue replicateswere retained for twoof thefourspecieslistedhere(Chaetodon lineolatusandChaetodon lunula)
Our Bayesian and maximum likelihood analyses produced afully resolvedtopologythatsharedkeypointsofcongruencewithpriormulti-locus studies of butterflyfishes (Bellwood et al 2010
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
AbererA JKobertKampStamatakisA (2014)ExaBayesMassivelyparallelBayesiantreeinferenceforthewhole-genomeeraMolecular Biology and Evolution 31 2553ndash2556 httpsdoiorg101093molbevmsu236
AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp10993DIBATTISTA eT Al
Spec
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ColorsinthetableheadermatchthecolorsusedtodenotespeciesdistributionsinFigure1AsterisksindicateregionalendemicsforthepurposesofourcorrelationaltraitanalysisThelettersbeloweach
regionindicatethegeographicgroupingsusedforBioGeoBEARSanalysisAlthoughC
haet
odon
leuc
ople
uraC
haet
odon
mel
aptu
rusand
Chae
todo
n pi
ctusarelistedasbeingpresentintheRedSeathisis
basedonrarerecordsattheirnorthernlimitsSimilarlywehaveonlysampledC
pic
tus(andnotC
haet
odon
vag
abun
dus)atSocotra(DiBattistaetal2017)andrarerecordsofC
haet
odon
aus
tria
cusinthe
GulfofAdenandSouthOmanlikelyrepresentwaifs
TAB
LE 1
emsp(Continued)
10994emsp |emsp emspensp DIBATTISTA eT Al
anddeep(Alfaroetal2018Fairclothetal2013Harringtonetal2016)phylogeneticscales
23emsp|emspDNA library preparation and next‐generation sequencing
DNA was extracted with DNeasy Blood and Tissue kits (QiagenValenciaCA)whichincludedanRNAseAtreatmentstepEachex-tractedsamplewasvisualizedbygelelectrophoresistoassessDNAqualityTotalDNAfromeachextractedaliquotwasquantifiedusingaQubitdsDNAHSAssayKit(InvitrogenCarlsbadCA)and12microgofDNAperindividualsamplewasfragmentedbysonicationto500basepairs (bp)usingaCovarisS2 sonicator (Covaris IncWoburnMA)andusedforUCElibrarypreparationInbriefweend-repairedadenylated and ligated fragmentedDNA to Illumina TruSeq-styleadapters which included custom sequence tags to barcode eachindividualsample (FairclothampGlenn2012)Followingan18-cyclePCRtoamplify indexed libraries forenrichmentwecreatedpoolsbycombining625ngofeightindividuallibrariesEachpoolwascon-centratedto147ngμlusingavacuumcentrifugeWethenfollowedanestablishedworkflowfortargetenrichment(Gnirkeetal2009)withmodificationsspecifiedinFairclothetal(2012)SpecificallyweenrichedeachpooltargetingUCElociandtheirflankingsequenceusingsyntheticRNAcaptureprobes(MyBaitsMycroarrayIncAnnArborMI)We combined the enriched indexed pools at equimo-lar ratios prior to sequencing The two final pooled librarieswereeach runpaired-end (150bpsequencing)on independent lanesofanIlluminaHiSeq2000(v3reagents)attheKAUSTBioscienceCoreLabDetailedmethodsoflibraryenrichmentpost-enrichmentPCRandvalidationusingrelativeqPCRmaybefoundathttpsultracon-servedorgprotocols
24emsp|emspSequence read quality control assembly and UCE identification
Weremovedadaptercontaminationand lowqualitybaseswith il-lumiprocessor (Faircloth2013)aparallelwrappertoTrimmomatic(BolgerLohseampUsadel2014)ToassemblethetrimmeddatasetweusedthePHYLUCEpipeline (version8ca5884Faircloth2016)with the phyluce_assembly_assemblo_trinitypywrapper script forTrinity(version150Grabherretal2011)WematchedassembledcontigstoenrichedUCElocibyaligningcontigsfromeachspeciesto our UCE probes using the phyluce_assembly_match_contigs_to_probespy scriptwith the LASTZ assembler (Harris 2007)WestoredthesematchresultsintoaSQLiterelationaldatabaseafterex-cludingcontigsthatmatchedmultipleUCElociandUCElociwhoseprobesmatchedmultiplecontigs
Weusedphyluce_align_seqcappytoalignUCElociwithMAFFT(Katohamp Standley 2013KatohMisawaKumaampMiyata 2002)Following alignment we end- and internally-trimmed alignmentswithGBLOCKS (Castresana 2000) to improvephylogenetic infer-encebyremovingpoorlyalignedorhighlydivergentsites(TalaveraampCastresana2007)Weselectedlocithatwerepresentinatleast
75 of our specimens and concatenated the alignments into aPHYLIP-formatted matrix for phylogenetic analysis We includedpreviouslypublishedUCEdataforthreespeciesinouralignmenttorepresentAcanthomorpha outgroup lineages andmore accuratelycalibratethephylogeny(seebelow)
25emsp|emspPhylogenetic analysis of concatenated UCE data evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
WefullypartitionedourconcatenatedalignmentbyUCElocusandperformedBayesiananalysesofthedatasetwithExaBayes(AbererKobert amp Stamatakis 2014) and two independent runs samplingevery500generationsWeusedtheautostoppingconvergencecri-teriaof anaverage standarddeviationof split frequenciesoflt5and visualized the log-likelihood of each chain to ensure conver-genceinTracerversion16(Rambautetal2014)
WeestimateddivergencetimesusingMCMCTREEinthePAMLpackage on the Bayesian consensus topologyWe used the likeli-hood approximation approach following the two-step proceduredescribedbyDosReis andYang (2011) by first estimating ameansubstitutionratefortheentirealignmentwithBASEMLunderastrictmolecularclockandthenusingthisestimatetosetthergene_priorinMCMCTREEWeusedasingleunpartitionedalignmentforcom-putationaltractabilitywithanHKY85modelfivecategoriesforthegammadistributionofrateheterogeneityanrgene_gammapriorforthe gamma distribution describing gene rate heterogeneity of (237105751)andasigma2_gammapriorof (251)WeadoptedacalibrationstrategythatbuildsonHarringtonetal(2016)byinclud-ingmoreproximalacanthomorphoutgroupstoChaetodontidaeandtheirimmediaterelativesWeconstrainedsixnodesonthebasisoffossilinformationusinghardlowerandsoftupperboundsoutlinedinSupportingInformationFigureS1Weassignedaminimumamountofpriorweightforagesbelowthelowerbound(1e-200)and5priorweightforageshigherthantheupperboundBrieflywelinkaseriesofcarangimorphsyngnathiformholocentroidandlampridiformfossilstothesequencesofacanthomorphoutgroupfossilsasperHarringtonet al (2016) This resulted in the following outgroup node calibra-tions acanthuroids versus all other taxa (lower bound 5417Maupperbound7084Ma)acanthuridsversuszanclids (lowerbound490Ma upper bound 627Ma) Naso versus Acanthurus (lowerbound 490Ma upper bound 5722Ma) Chaetodontidae versusPomacanthidae (lower bound 2962Ma upper bound 5926Ma)and the total-group Chaetodon versus Prognathodes (lower bound7Maupperbound475Ma)FurtherjustificationforcalibrationsisavailableasSupportingInformation(AppendixS1)
26emsp|emspAncestral biogeographic range estimation evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Weestimatedancestraldistributionpatterns forchaetodontid lin-eages using the pruned time-calibrated phylogeny analyzed with
emspensp emsp | emsp10995DIBATTISTA eT Al
theRpackageBioGeoBEARS(Matzke2013)whichallowsseveralmodels of biogeographic evolution to be compared via likelihoodinference and the ability to incorporate a parameter allowing forfounder-eventspeciationFortheseanalyseswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareasGulfofAqabarestoftheRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPOThediscretecodingofgeographicareasadjacenttotheArabianPeninsulaenablesafine-scaleinvestigationoftheances-tralbiogeographyofthatregionforourtaxaofinterestPresenceabsenceandgeographicalrangedataforeachtaxonwereobtainedfromacombinationofDiBattistaRobertsetal(2016)andFishBase(FroeseampPauly2011)Prognathodesspp(aChaetodontidaegenus)werenotconsideredinthispartoftheanalysisgiventhatthesetwotaxaarerestrictedtotropicalAtlanticwaters
Weconstrainedourbiogeographicanalysestoprohibitcoloniza-tioneventsbetweentheRedSeaandIndianPOregionsbefore5Mareflectingthetimewhenamorepermanentconnectionwasformedvia theStraitofBabalMandab (Bailey2010)OurBioGeoBEARSanalysis evaluated the DEC DIVALIKE and BAYAREALIKE mod-elswithandwithoutthejump(J)parameter(Matzke2013)Thesemodels describe biogeographic scenarios where dispersal extinc-tioncladogenesisvicarianceandfoundereventsaredifferentiallyinvokedtoexplainpresentdaydistributionalpatterns Inourcasewewereinterestedinwhethertherange-restrictedendemicsfromthecoastalwatersoftheArabianPeninsularepresentancientrelictsnew colonization events andor a sourceof biodiversity (at somepointinthepast)forthebroaderIndo-WestPacific
27emsp|emspComparative trait analysis evaluation of the ldquoecological traitrdquo hypothesis
In order to determine whether particular species-level traitswere associatedwith the evolutionof endemism in this subset ofChaetodontidaespecieswefittedaphylogeneticgeneralizedlinearmodel(functionldquophyloglmrdquoinRpackageldquophylolmrdquo[Hoetal2016])thatassumedldquoregionalendemismrdquo(ieendemictothecoastalwa-tersoftheArabianPeninsulaDiBattistaRobertsetal2016)asthebinomialresponsevariableandasuiteofecologicaltraitsasthepre-dictivefixedfactorsFormodelselectionweperformedabackwardstepwiseprocedureforPGLMrsquos(functionldquophylosteprdquoinRpackageldquophylolmrdquo[Hoetal2016])whichentailedsequentialoptimizationbyremovingnon-influentialfixed-effecttermsfromthefullmodelbasedonAkaikeinformationcriteria(AIC)Fulldetailsonthemeth-odsanddatasourcesareprovidedinSupportingInformationTableS2Wealsoexplore interactionsamongthepredictivetraitsusinga regression tree approach (Dersquoath and Fabricius 2000 functionldquorpartrdquoinRpackageldquorpartrdquo[Therneauetal2015])
Amongthepredictivevariablesconsideredweremaximumbodysize(totallength=TLAllenetal1998Kuiter2002)depthrangeinhabited (Allenet al1998) social structure (threecategoriesor-deredfromlowtohighsociabilitysolitarypairformationandgroupformation Allen et al 1998 Kuiter 2002 Yabuta and Berumen
2013) habitat breadth (estimated as the sum value of all habitattypes inhabited C=coral R=rocky D=deep reef S=sedimentR=rubbleCO=coastalCA=algalbedsAllenetal1998Kuiter2002)anddietaryrelianceoncoral reefs (fourcategoriesorderedfromlowtohighrelianceplanktivorebenthicinvertivorefaculta-tivecorallivoreandobligatecorallivoreColeandPratchett2014)Wealsoincludedthephylogeneticageofspecies(Myr)asanaddi-tional fixedfactor totestwhetherspecies traitsare influencedbytimeofdivergencefromsistertaxaForphylogeneticageweeval-uate for each species (regional endemic andwidespread)whetherwe sampled its closest sister speciesby comparingourphylogenywith those published previously (CowmanampBellwood 2011) andotherpublishedaccounts(Kuiter2002)Theecologicaltraitswereselected because they are associated with specialization fitnessandrangeexpansioninbutterflyfishesandthusmayhelptoexplainpatternsofevolutioninfishendemictothecoralreefsoftheArabianPeninsulaWedonotethismaybeanoversimplificationgiventhatourcategoriesarecoarseandbiasedtowardadultversuslarvaltraitswhichare themselvesdatadeficientPreviousworkhoweverhasdemonstratedthattraitsassociatedwiththesuccessfulrecruitmentofreeffisharemoreimportantthantraitsassociatedwithdispersalindeterminingdifferentiationbetweenhabitats(Gaitheretal2015KeithWoolseyMadinByrneampBaird2015)
3emsp |emspRESULTS
31emsp|emspUCE sequences
ReadscontigsandUCElociperindividualareoutlinedinSupportingInformationTableS3Insummarywesequencedatotalof15331millionreadswithameanof155millionreadspersamplefrom47focaltaxa(excludingoutgroupsalsoseeTable1)Overallweassem-bledameanof12969contigs(95CImin=10593max=15345)and901UCElocipersample(95CImin=871max=932)
32emsp|emspPhylogenetic reconstruction and timing of divergence evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Followingassemblyalignmenttrimmingandfilteringoutlocithatwerepresentinfewerthan75specimens(fora75completedata-set)we retained971 alignmentswith amean length of 5156bpThe concatenated supermatrix contained500642bpwith52680informativesitesandwas833completebasedontheproportionofnon-gapsequencesThefollowingsampleswereexcludedfromfurtheranalysisduetothelownumberoflocirecoveredChaetodon_interruptus1a Chaetodon_lineolatus1a Chaetodon_lunula1a andChaetodon ulietensis1a (for full details see Supporting InformationTableS1) however tissue replicateswere retained for twoof thefourspecieslistedhere(Chaetodon lineolatusandChaetodon lunula)
Our Bayesian and maximum likelihood analyses produced afully resolvedtopologythatsharedkeypointsofcongruencewithpriormulti-locus studies of butterflyfishes (Bellwood et al 2010
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
AbererA JKobertKampStamatakisA (2014)ExaBayesMassivelyparallelBayesiantreeinferenceforthewhole-genomeeraMolecular Biology and Evolution 31 2553ndash2556 httpsdoiorg101093molbevmsu236
AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
10994emsp |emsp emspensp DIBATTISTA eT Al
anddeep(Alfaroetal2018Fairclothetal2013Harringtonetal2016)phylogeneticscales
23emsp|emspDNA library preparation and next‐generation sequencing
DNA was extracted with DNeasy Blood and Tissue kits (QiagenValenciaCA)whichincludedanRNAseAtreatmentstepEachex-tractedsamplewasvisualizedbygelelectrophoresistoassessDNAqualityTotalDNAfromeachextractedaliquotwasquantifiedusingaQubitdsDNAHSAssayKit(InvitrogenCarlsbadCA)and12microgofDNAperindividualsamplewasfragmentedbysonicationto500basepairs (bp)usingaCovarisS2 sonicator (Covaris IncWoburnMA)andusedforUCElibrarypreparationInbriefweend-repairedadenylated and ligated fragmentedDNA to Illumina TruSeq-styleadapters which included custom sequence tags to barcode eachindividualsample (FairclothampGlenn2012)Followingan18-cyclePCRtoamplify indexed libraries forenrichmentwecreatedpoolsbycombining625ngofeightindividuallibrariesEachpoolwascon-centratedto147ngμlusingavacuumcentrifugeWethenfollowedanestablishedworkflowfortargetenrichment(Gnirkeetal2009)withmodificationsspecifiedinFairclothetal(2012)SpecificallyweenrichedeachpooltargetingUCElociandtheirflankingsequenceusingsyntheticRNAcaptureprobes(MyBaitsMycroarrayIncAnnArborMI)We combined the enriched indexed pools at equimo-lar ratios prior to sequencing The two final pooled librarieswereeach runpaired-end (150bpsequencing)on independent lanesofanIlluminaHiSeq2000(v3reagents)attheKAUSTBioscienceCoreLabDetailedmethodsoflibraryenrichmentpost-enrichmentPCRandvalidationusingrelativeqPCRmaybefoundathttpsultracon-servedorgprotocols
24emsp|emspSequence read quality control assembly and UCE identification
Weremovedadaptercontaminationand lowqualitybaseswith il-lumiprocessor (Faircloth2013)aparallelwrappertoTrimmomatic(BolgerLohseampUsadel2014)ToassemblethetrimmeddatasetweusedthePHYLUCEpipeline (version8ca5884Faircloth2016)with the phyluce_assembly_assemblo_trinitypywrapper script forTrinity(version150Grabherretal2011)WematchedassembledcontigstoenrichedUCElocibyaligningcontigsfromeachspeciesto our UCE probes using the phyluce_assembly_match_contigs_to_probespy scriptwith the LASTZ assembler (Harris 2007)WestoredthesematchresultsintoaSQLiterelationaldatabaseafterex-cludingcontigsthatmatchedmultipleUCElociandUCElociwhoseprobesmatchedmultiplecontigs
Weusedphyluce_align_seqcappytoalignUCElociwithMAFFT(Katohamp Standley 2013KatohMisawaKumaampMiyata 2002)Following alignment we end- and internally-trimmed alignmentswithGBLOCKS (Castresana 2000) to improvephylogenetic infer-encebyremovingpoorlyalignedorhighlydivergentsites(TalaveraampCastresana2007)Weselectedlocithatwerepresentinatleast
75 of our specimens and concatenated the alignments into aPHYLIP-formatted matrix for phylogenetic analysis We includedpreviouslypublishedUCEdataforthreespeciesinouralignmenttorepresentAcanthomorpha outgroup lineages andmore accuratelycalibratethephylogeny(seebelow)
25emsp|emspPhylogenetic analysis of concatenated UCE data evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
WefullypartitionedourconcatenatedalignmentbyUCElocusandperformedBayesiananalysesofthedatasetwithExaBayes(AbererKobert amp Stamatakis 2014) and two independent runs samplingevery500generationsWeusedtheautostoppingconvergencecri-teriaof anaverage standarddeviationof split frequenciesoflt5and visualized the log-likelihood of each chain to ensure conver-genceinTracerversion16(Rambautetal2014)
WeestimateddivergencetimesusingMCMCTREEinthePAMLpackage on the Bayesian consensus topologyWe used the likeli-hood approximation approach following the two-step proceduredescribedbyDosReis andYang (2011) by first estimating ameansubstitutionratefortheentirealignmentwithBASEMLunderastrictmolecularclockandthenusingthisestimatetosetthergene_priorinMCMCTREEWeusedasingleunpartitionedalignmentforcom-putationaltractabilitywithanHKY85modelfivecategoriesforthegammadistributionofrateheterogeneityanrgene_gammapriorforthe gamma distribution describing gene rate heterogeneity of (237105751)andasigma2_gammapriorof (251)WeadoptedacalibrationstrategythatbuildsonHarringtonetal(2016)byinclud-ingmoreproximalacanthomorphoutgroupstoChaetodontidaeandtheirimmediaterelativesWeconstrainedsixnodesonthebasisoffossilinformationusinghardlowerandsoftupperboundsoutlinedinSupportingInformationFigureS1Weassignedaminimumamountofpriorweightforagesbelowthelowerbound(1e-200)and5priorweightforageshigherthantheupperboundBrieflywelinkaseriesofcarangimorphsyngnathiformholocentroidandlampridiformfossilstothesequencesofacanthomorphoutgroupfossilsasperHarringtonet al (2016) This resulted in the following outgroup node calibra-tions acanthuroids versus all other taxa (lower bound 5417Maupperbound7084Ma)acanthuridsversuszanclids (lowerbound490Ma upper bound 627Ma) Naso versus Acanthurus (lowerbound 490Ma upper bound 5722Ma) Chaetodontidae versusPomacanthidae (lower bound 2962Ma upper bound 5926Ma)and the total-group Chaetodon versus Prognathodes (lower bound7Maupperbound475Ma)FurtherjustificationforcalibrationsisavailableasSupportingInformation(AppendixS1)
26emsp|emspAncestral biogeographic range estimation evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Weestimatedancestraldistributionpatterns forchaetodontid lin-eages using the pruned time-calibrated phylogeny analyzed with
emspensp emsp | emsp10995DIBATTISTA eT Al
theRpackageBioGeoBEARS(Matzke2013)whichallowsseveralmodels of biogeographic evolution to be compared via likelihoodinference and the ability to incorporate a parameter allowing forfounder-eventspeciationFortheseanalyseswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareasGulfofAqabarestoftheRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPOThediscretecodingofgeographicareasadjacenttotheArabianPeninsulaenablesafine-scaleinvestigationoftheances-tralbiogeographyofthatregionforourtaxaofinterestPresenceabsenceandgeographicalrangedataforeachtaxonwereobtainedfromacombinationofDiBattistaRobertsetal(2016)andFishBase(FroeseampPauly2011)Prognathodesspp(aChaetodontidaegenus)werenotconsideredinthispartoftheanalysisgiventhatthesetwotaxaarerestrictedtotropicalAtlanticwaters
Weconstrainedourbiogeographicanalysestoprohibitcoloniza-tioneventsbetweentheRedSeaandIndianPOregionsbefore5Mareflectingthetimewhenamorepermanentconnectionwasformedvia theStraitofBabalMandab (Bailey2010)OurBioGeoBEARSanalysis evaluated the DEC DIVALIKE and BAYAREALIKE mod-elswithandwithoutthejump(J)parameter(Matzke2013)Thesemodels describe biogeographic scenarios where dispersal extinc-tioncladogenesisvicarianceandfoundereventsaredifferentiallyinvokedtoexplainpresentdaydistributionalpatterns Inourcasewewereinterestedinwhethertherange-restrictedendemicsfromthecoastalwatersoftheArabianPeninsularepresentancientrelictsnew colonization events andor a sourceof biodiversity (at somepointinthepast)forthebroaderIndo-WestPacific
27emsp|emspComparative trait analysis evaluation of the ldquoecological traitrdquo hypothesis
In order to determine whether particular species-level traitswere associatedwith the evolutionof endemism in this subset ofChaetodontidaespecieswefittedaphylogeneticgeneralizedlinearmodel(functionldquophyloglmrdquoinRpackageldquophylolmrdquo[Hoetal2016])thatassumedldquoregionalendemismrdquo(ieendemictothecoastalwa-tersoftheArabianPeninsulaDiBattistaRobertsetal2016)asthebinomialresponsevariableandasuiteofecologicaltraitsasthepre-dictivefixedfactorsFormodelselectionweperformedabackwardstepwiseprocedureforPGLMrsquos(functionldquophylosteprdquoinRpackageldquophylolmrdquo[Hoetal2016])whichentailedsequentialoptimizationbyremovingnon-influentialfixed-effecttermsfromthefullmodelbasedonAkaikeinformationcriteria(AIC)Fulldetailsonthemeth-odsanddatasourcesareprovidedinSupportingInformationTableS2Wealsoexplore interactionsamongthepredictivetraitsusinga regression tree approach (Dersquoath and Fabricius 2000 functionldquorpartrdquoinRpackageldquorpartrdquo[Therneauetal2015])
Amongthepredictivevariablesconsideredweremaximumbodysize(totallength=TLAllenetal1998Kuiter2002)depthrangeinhabited (Allenet al1998) social structure (threecategoriesor-deredfromlowtohighsociabilitysolitarypairformationandgroupformation Allen et al 1998 Kuiter 2002 Yabuta and Berumen
2013) habitat breadth (estimated as the sum value of all habitattypes inhabited C=coral R=rocky D=deep reef S=sedimentR=rubbleCO=coastalCA=algalbedsAllenetal1998Kuiter2002)anddietaryrelianceoncoral reefs (fourcategoriesorderedfromlowtohighrelianceplanktivorebenthicinvertivorefaculta-tivecorallivoreandobligatecorallivoreColeandPratchett2014)Wealsoincludedthephylogeneticageofspecies(Myr)asanaddi-tional fixedfactor totestwhetherspecies traitsare influencedbytimeofdivergencefromsistertaxaForphylogeneticageweeval-uate for each species (regional endemic andwidespread)whetherwe sampled its closest sister speciesby comparingourphylogenywith those published previously (CowmanampBellwood 2011) andotherpublishedaccounts(Kuiter2002)Theecologicaltraitswereselected because they are associated with specialization fitnessandrangeexpansioninbutterflyfishesandthusmayhelptoexplainpatternsofevolutioninfishendemictothecoralreefsoftheArabianPeninsulaWedonotethismaybeanoversimplificationgiventhatourcategoriesarecoarseandbiasedtowardadultversuslarvaltraitswhichare themselvesdatadeficientPreviousworkhoweverhasdemonstratedthattraitsassociatedwiththesuccessfulrecruitmentofreeffisharemoreimportantthantraitsassociatedwithdispersalindeterminingdifferentiationbetweenhabitats(Gaitheretal2015KeithWoolseyMadinByrneampBaird2015)
3emsp |emspRESULTS
31emsp|emspUCE sequences
ReadscontigsandUCElociperindividualareoutlinedinSupportingInformationTableS3Insummarywesequencedatotalof15331millionreadswithameanof155millionreadspersamplefrom47focaltaxa(excludingoutgroupsalsoseeTable1)Overallweassem-bledameanof12969contigs(95CImin=10593max=15345)and901UCElocipersample(95CImin=871max=932)
32emsp|emspPhylogenetic reconstruction and timing of divergence evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Followingassemblyalignmenttrimmingandfilteringoutlocithatwerepresentinfewerthan75specimens(fora75completedata-set)we retained971 alignmentswith amean length of 5156bpThe concatenated supermatrix contained500642bpwith52680informativesitesandwas833completebasedontheproportionofnon-gapsequencesThefollowingsampleswereexcludedfromfurtheranalysisduetothelownumberoflocirecoveredChaetodon_interruptus1a Chaetodon_lineolatus1a Chaetodon_lunula1a andChaetodon ulietensis1a (for full details see Supporting InformationTableS1) however tissue replicateswere retained for twoof thefourspecieslistedhere(Chaetodon lineolatusandChaetodon lunula)
Our Bayesian and maximum likelihood analyses produced afully resolvedtopologythatsharedkeypointsofcongruencewithpriormulti-locus studies of butterflyfishes (Bellwood et al 2010
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
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AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
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Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
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Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
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BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
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ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
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CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
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KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
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McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
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Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp10995DIBATTISTA eT Al
theRpackageBioGeoBEARS(Matzke2013)whichallowsseveralmodels of biogeographic evolution to be compared via likelihoodinference and the ability to incorporate a parameter allowing forfounder-eventspeciationFortheseanalyseswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareasGulfofAqabarestoftheRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPOThediscretecodingofgeographicareasadjacenttotheArabianPeninsulaenablesafine-scaleinvestigationoftheances-tralbiogeographyofthatregionforourtaxaofinterestPresenceabsenceandgeographicalrangedataforeachtaxonwereobtainedfromacombinationofDiBattistaRobertsetal(2016)andFishBase(FroeseampPauly2011)Prognathodesspp(aChaetodontidaegenus)werenotconsideredinthispartoftheanalysisgiventhatthesetwotaxaarerestrictedtotropicalAtlanticwaters
Weconstrainedourbiogeographicanalysestoprohibitcoloniza-tioneventsbetweentheRedSeaandIndianPOregionsbefore5Mareflectingthetimewhenamorepermanentconnectionwasformedvia theStraitofBabalMandab (Bailey2010)OurBioGeoBEARSanalysis evaluated the DEC DIVALIKE and BAYAREALIKE mod-elswithandwithoutthejump(J)parameter(Matzke2013)Thesemodels describe biogeographic scenarios where dispersal extinc-tioncladogenesisvicarianceandfoundereventsaredifferentiallyinvokedtoexplainpresentdaydistributionalpatterns Inourcasewewereinterestedinwhethertherange-restrictedendemicsfromthecoastalwatersoftheArabianPeninsularepresentancientrelictsnew colonization events andor a sourceof biodiversity (at somepointinthepast)forthebroaderIndo-WestPacific
27emsp|emspComparative trait analysis evaluation of the ldquoecological traitrdquo hypothesis
In order to determine whether particular species-level traitswere associatedwith the evolutionof endemism in this subset ofChaetodontidaespecieswefittedaphylogeneticgeneralizedlinearmodel(functionldquophyloglmrdquoinRpackageldquophylolmrdquo[Hoetal2016])thatassumedldquoregionalendemismrdquo(ieendemictothecoastalwa-tersoftheArabianPeninsulaDiBattistaRobertsetal2016)asthebinomialresponsevariableandasuiteofecologicaltraitsasthepre-dictivefixedfactorsFormodelselectionweperformedabackwardstepwiseprocedureforPGLMrsquos(functionldquophylosteprdquoinRpackageldquophylolmrdquo[Hoetal2016])whichentailedsequentialoptimizationbyremovingnon-influentialfixed-effecttermsfromthefullmodelbasedonAkaikeinformationcriteria(AIC)Fulldetailsonthemeth-odsanddatasourcesareprovidedinSupportingInformationTableS2Wealsoexplore interactionsamongthepredictivetraitsusinga regression tree approach (Dersquoath and Fabricius 2000 functionldquorpartrdquoinRpackageldquorpartrdquo[Therneauetal2015])
Amongthepredictivevariablesconsideredweremaximumbodysize(totallength=TLAllenetal1998Kuiter2002)depthrangeinhabited (Allenet al1998) social structure (threecategoriesor-deredfromlowtohighsociabilitysolitarypairformationandgroupformation Allen et al 1998 Kuiter 2002 Yabuta and Berumen
2013) habitat breadth (estimated as the sum value of all habitattypes inhabited C=coral R=rocky D=deep reef S=sedimentR=rubbleCO=coastalCA=algalbedsAllenetal1998Kuiter2002)anddietaryrelianceoncoral reefs (fourcategoriesorderedfromlowtohighrelianceplanktivorebenthicinvertivorefaculta-tivecorallivoreandobligatecorallivoreColeandPratchett2014)Wealsoincludedthephylogeneticageofspecies(Myr)asanaddi-tional fixedfactor totestwhetherspecies traitsare influencedbytimeofdivergencefromsistertaxaForphylogeneticageweeval-uate for each species (regional endemic andwidespread)whetherwe sampled its closest sister speciesby comparingourphylogenywith those published previously (CowmanampBellwood 2011) andotherpublishedaccounts(Kuiter2002)Theecologicaltraitswereselected because they are associated with specialization fitnessandrangeexpansioninbutterflyfishesandthusmayhelptoexplainpatternsofevolutioninfishendemictothecoralreefsoftheArabianPeninsulaWedonotethismaybeanoversimplificationgiventhatourcategoriesarecoarseandbiasedtowardadultversuslarvaltraitswhichare themselvesdatadeficientPreviousworkhoweverhasdemonstratedthattraitsassociatedwiththesuccessfulrecruitmentofreeffisharemoreimportantthantraitsassociatedwithdispersalindeterminingdifferentiationbetweenhabitats(Gaitheretal2015KeithWoolseyMadinByrneampBaird2015)
3emsp |emspRESULTS
31emsp|emspUCE sequences
ReadscontigsandUCElociperindividualareoutlinedinSupportingInformationTableS3Insummarywesequencedatotalof15331millionreadswithameanof155millionreadspersamplefrom47focaltaxa(excludingoutgroupsalsoseeTable1)Overallweassem-bledameanof12969contigs(95CImin=10593max=15345)and901UCElocipersample(95CImin=871max=932)
32emsp|emspPhylogenetic reconstruction and timing of divergence evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Followingassemblyalignmenttrimmingandfilteringoutlocithatwerepresentinfewerthan75specimens(fora75completedata-set)we retained971 alignmentswith amean length of 5156bpThe concatenated supermatrix contained500642bpwith52680informativesitesandwas833completebasedontheproportionofnon-gapsequencesThefollowingsampleswereexcludedfromfurtheranalysisduetothelownumberoflocirecoveredChaetodon_interruptus1a Chaetodon_lineolatus1a Chaetodon_lunula1a andChaetodon ulietensis1a (for full details see Supporting InformationTableS1) however tissue replicateswere retained for twoof thefourspecieslistedhere(Chaetodon lineolatusandChaetodon lunula)
Our Bayesian and maximum likelihood analyses produced afully resolvedtopologythatsharedkeypointsofcongruencewithpriormulti-locus studies of butterflyfishes (Bellwood et al 2010
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
AbererA JKobertKampStamatakisA (2014)ExaBayesMassivelyparallelBayesiantreeinferenceforthewhole-genomeeraMolecular Biology and Evolution 31 2553ndash2556 httpsdoiorg101093molbevmsu236
AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
10996emsp |emsp emspensp DIBATTISTA eT Al
CowmanampBellwood 2011 FesslerampWestneat 2007Hodge etal2014Hsuetal2007seeSupportingInformationFigureS2)Although direct comparisons to previous phylogenies are difficultbecause these are missing many of the regional endemics (egChaetodon dialeucos C gardineri C leucopleura C nigropunctatusC pictusC triangulumHeniochus intermedius)andcontain lessse-quencedataanddataoverlap(egsixlociand73completematrixHodgeet al 2014)where therewasoverlap in thedata sets thetipsofthetreedisplayedsimilartopologies(SupportingInformation
FigureS3)Inourcasehoweveralmosteverynodeinthetreewasstronglysupported(posteriorprobabilitiesof10Figures1and2)
Byonlyconsideringasingle representativesampleperspecieson our chronogram (Figure 2)we found that themajority of RedSea toArabianGulfbutterflyfishdiverged from their closest rela-tives in the last fivemillion years (417ndash116Ma)with an averagelineageageof239Ma Incomparisontopreviousfossilcalibratedstudies ofChaetodontidae (CowmanampBellwood 2011Hodge etal2014)themeanagesand95highestposteriordensity(HPD)
F I G U R E 1 emsp InferredphylogenyofRedSeatoArabianGulfbutterflyfishspeciesincludingsomeofclosesttheircongenersbasedonExaBayesanalysisofultraconservedelementdataYellowdotsonnodelabelsindicateaposteriorprobabilityof1whereasgraydotsindicateaposteriorprobabilityoflt1butgt06CladesbasedonBellwoodetal(2010)andCowmanandBellwood(2011)areindicatedRecordsforeachspeciesaremappedontothetopologyasfollowsred=RedSeatoArabianGulfgreen=restofIndianOceanandblue=PacificOcean
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
Chaetodon pictus 2
Chaetodon decussatus
Chaetodon pictus 2bChaetodon pictus 1a
Chaetodon pictus 1Chaetodon vagabundus 1a
Chaetodon vagabundus 2b
Chaetodon vagabundus 2
Chaetodon vagabundus 1
Chaetodon auriga 1
Chaetodon auriga 2
Chaetodon nigropunctatus 2b
Chaetodon nigropunctatus
Chaetodon nigropunctatus 3c
Chaetodon nigropunctatus 1a
Chaetodon m
esoleucos 2
Chaetodon mesoleucos 1
Chaetodon dialeucos 1
Chaetodon dialeucos 2
Chaetodon lineolatus 1
Chaetodon lineolatus 2
Chaetodon oxycephalus 1a
Chaetodon falcula
Chaetod
on semilarvatus 2
Chaetodon sem
ilarvatus 1
2 al
unul
nodo
teah
C Chaetod
on lunula 1
Cha
etod
on u
nim
acul
atus
1ab2 sutaluca
minu nodoteahC Cha
etod
on u
nim
acul
atus
Pro
gnat
hode
s ac
ulea
tus
Pro
gnat
hode
s m
arce
llae
Forc
ipig
er fl
avis
sim
us 3
c
Forc
ipig
er fl
avis
sim
us 2
bFo
rcip
iger
flav
issi
mus
2
Forc
ipig
er fl
avis
sim
us 1
Forc
ipig
er fl
avis
sim
us 1
a
Forc
ipig
er lo
ngiro
stris
Forc
ipig
er lo
ngiro
stris
1a
Heniochus interm
edius
Henioch
us diphreu
tes 2b
Henioc
hus a
cum
inatu
s 2b
Henio
chus
dip
hreu
tes
Heniochus diphreutes 1
a
Cha
etod
on fa
scia
tus
1C
haet
odon
fasc
iatu
s 2
Cha
etod
on a
urip
es
Cha
etod
on c
olla
re 2
Cha
etod
on c
olla
re 1
Cha
etod
on c
olla
re 1
a
Cha
etod
on m
elan
notu
s 2b
Cha
etod
on m
elan
notu
s 1a
Cha
etod
on m
elan
notu
s 2
Cha
etod
on m
elan
notu
s 1
Chaet
odon
leuc
opleu
ra 2
Chaet
odon
leuc
ople
ura
1
Chaet
odon
gar
dine
ri
Chaetodon speculum 1a
Chaetodon speculum 2b
Chaetodon za
nzibare
nsis 2
Chaeto
don zan
zibare
nsis
1Chaetodon bennetti 2
Chaetodon bennetti 1Chaetodon plebeius
Chaetodon trifascialis 1a
Chaetodon trifascialis 2Chaetodon trifascialis 1
Chaetodon baronessa
Chaetodon triangulum 1a
Chaetodon triangulum 2b
Chaetodon larvatus 1Chaetodon larvatus 2
Chaetodon austriacus 2Chaetodon melapterus 1
Chaetodon austriacus 1
Chaetodon melapterus 2
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon xanthurus 2b
Chaetodon xanthurus 1a
Chaetodon paucifasciatus 2
Chaetodon paucifasciatus 1C
haetodon madagaskariensis
Chaetodon m
ertensiiChaetodon guttatissimus 1a
Chaetodon guttatissimus 1
Chaetodon guttatissimus 4d
Chaetodon guttatissimus 3c
Chaetodon pelewensis
Chaetodon punctatofasciatus 1a
Chaetodon trichrous
Chaetodon kleinii 2b
Chaetodon kleinii 2
Chaetodon kleinii 3c
Chaetod
on kleinii 1a
Chaetod
on kleinii 1
Clade CH2
Clad
e CH
3Clade CH4
Bannerfishes
Pomacanthus paru
Acanthurus olivaceus
Naso unicornis
Zanclus cornutus
Platax orbicularis 1Platax orbicularis 2
Istiophorus platypterusMene maculatus
Bothus pantherinus
Red S
ea to Arabian G
ul fIInnddiiiaaann
OOOOOccceeeaaaaannn
PPPaaaccccciiifffiiiccc
OOOOOccceeeaaaaannn
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
287
154
103
98
67
43
4
35
25
2
16
2
16
31
26
22
32
27
17
43
12
83
66
58
33
3
18
29
1
22
15
12
74
53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
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AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
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Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
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Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
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Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
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CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
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DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
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HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
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HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
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Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
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KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
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KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
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LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
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Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
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SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
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Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp10997DIBATTISTA eT Al
estimates aremore restricted but for themost part overlapwithpreviousestimates (Supporting InformationFigureS3) Intermsofthe topology although our phylogenetic sampling is restricted itstillcapturescrownnodesandageestimatesofmajorchaetodontidlineages (with the exception of the bannerfish lineage) aswell assubcladescontainingRedSeatoArabianGulfspeciesandtheirmost
recentcommonancestors(SupportingInformationFigureS2)Mostofthecladesincludedspeciespairsdivergingwithnon-overlappingdistributionsdatingback2ndash1MaThisdivergencedoesnotappeartocoincidewiththetimingoftheemergenceofapparentgeographic(andgeological)barrierssuchastheStraitofBabalMandab(Figures2and3)Regionalendemicsappeartohavedivergedearliestfrom
F I G U R E 2 emspAfossilcalibratedchronogramforselectChaetodontidaespeciesbasedonanalysisofultraconservedelementdataThetimescaleiscalibratedinmillionsofyearsbeforepresentNodeagesarepresentedasmediannodeheightswith95highestposteriordensityintervalsrepresentedbybarsSignificantgeologicaleventsinthecoastalwatersoftheArabianPeninsulaaretemporallyindicatedbyreddashedlines
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53
17
15
15
19
16
31
12
47
92
22
15
42
Ma45 40 35 30 25 20 15 10 5 0
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon fasciatus
Chaetodon lunula
Chaetodon auripes
Chaetodon collare
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon plebeius
Chaetodon trifascialis
Chaetodon baronessa
Chaetodon triangulum
Chaetodon larvatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon lunulatus
Chaetodon trifasciatus
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon unimaculatus
Prognathodes aculeatus
Prognathodes marcellae
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Forcipiger longirostris
Forcipiger flavissimus
Formation of the Red Sea basin
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Eocene Oligocene Miocene Plio PlePaleogene Neogene Q
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
AbererA JKobertKampStamatakisA (2014)ExaBayesMassivelyparallelBayesiantreeinferenceforthewhole-genomeeraMolecular Biology and Evolution 31 2553ndash2556 httpsdoiorg101093molbevmsu236
AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
10998emsp |emsp emspensp DIBATTISTA eT Al
F I G U R E 3 emspDistributionsrangeoverlapandagesofdivergenceineightcladesofbutterflyfishfromtheChaetodongenusthatcontainspeciesinhabitingtheRedSeatoArabianGulfregionCladestructureandnodeages(mediannodeheightswith95highestposteriordensityintervalsrepresentedbybars)wereextractedfromFigurethinsp2
2500 km
2500 km
2500 km
2500 km
(a)
(b)
(c)
(d)
C pictus
C decussatus
C vagabundus
C auriga
C mertensii
C madagaskariensis
C xanthurus
C paucifasciatus
C austriacus
C melapterus
C lunulatus
C baronessa
C triangulum
C larvatus
C trifasciatus
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
AbererA JKobertKampStamatakisA (2014)ExaBayesMassivelyparallelBayesiantreeinferenceforthewhole-genomeeraMolecular Biology and Evolution 31 2553ndash2556 httpsdoiorg101093molbevmsu236
AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp10999DIBATTISTA eT Al
ancestorsthatgaverisetotheclades includingChaetodon larvatus andChaetodon semilarvatusAtleastoneentiresubcladeofCH4wascomprisedofregionalendemics(C dialeucosC nigropunctatusand
C mesoleucos) The split between the butterflyfishes (ChaetodonPrognathodes) and bannerfishes (Heniochus Forcipiger) was mucholderwithameanof287Ma(95HPD400ndash1826Figure2and
2500 km
2500 km
2500 km
2500 km
(e)
(f)
(g)
(h)
C lunula
C fasciatus
C mesoleucos
C nigropunctatus
C dialeucos
C oxycephalus
C falcula
C lineolatus
C semilarvatus
C gardineri
C leucopleura
F I G U R E 3 emspContinued
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
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AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
11000emsp |emsp emspensp DIBATTISTA eT Al
Supporting Information Figure S1) indicating an ancient split be-tweenthesehighlydivergentbodyforms
33emsp|emspAncestral range reconstruction evaluation of the ldquoevolutionary incubatorrdquo and ldquoPleistocene extirpationrdquo hypotheses
Model comparison revealed the DEC+J model as the most likely(LnL=minus25079AICweight=076)andtheDIVALIKE+Jmodelasthesecondmost likely (LnL=minus25276AICweight=011 Table 2 andFigure4)The importanceof the J parameterwhichmodels long-distanceorldquojumprdquodispersalisthatancestralrangesoftencompriseonearearatherthanseveralareasTheadditionoftheJparameterresulted in a significantly better model fit for DECmodels whencomparedviaalikelihoodratiotest(LRTD = 867p = 00032)
Under theDEC+JmodelChaetodontidaehad their crownori-ginsintheIndo-WestPacificwithsubsequentdispersaltoincludetheArabianPeninsulaandlineagesleadingtothebaseofChaetodon andthebannerfishclade(ForcipigerHeniochusFigure4)WithintheCH2cladediversificationwasrestrictedtothePOwithsubsequentdispersaltotheIndianOcean(Chaetodon madagaskariensis C punc‐tatofasciaticus and C unimaculatus) and three of the species havedispersed as far as Socotra (Chaetodon guttatissimus C kleinii and C trifasciatus)OnlyonespecieswithinCH2divergedintheGulfofAdenandsubsequentlycolonizedtheRedSea(Chaetodon paucifas‐ciatus)TheageofC paucifasciatusisrelativelyyoung(15MaHPD08ndash23Ma)suggestingasimilar timelinefor itsoccupationoftheRedSeafromtheGulfofAden
IntheCH3cladethreespecieswerepresentintheRedSeathatwerealsorestrictedtotheArabianPeninsula(Chaetodon austriacus C melapterus and C larvatus)InthecaseofsisterpairC austriacus andC melapterus the reconstruction suggests that speciation oc-curredbyvicariancewithintheRedSeaAlthoughposteriorprob-abilities make the details of this split equivocal the most likelyscenario is a split between the Gulf of Aqaba and the Red SeawhereC austriacussubsequentlyrecolonizedtheentireRedSeabutC melapterus expandedout to theGulfofAdenArabianSeaand
ArabianGulfbutnofurtherTheextendedhistoryofthecladeal-thoughnotcompletelysampled(seeSupportingInformationFigureS2) suggests that a widespread ancestor expanded into the RedSeawithsubsequentvicariancebetweenthePOIndianOceanandArabianPeninsula sites IndeedC larvatus appears tooriginate inDjibouti and theGulf of Aden followed by dispersal into the RedSeaandSouthOmanChaetodon trifascialisontheotherhandmain-tained connections across the Indo-West Pacificwith subsequentrangeexpansionintotheRedSea
TheCH4cladehasbeenthemostsuccessfulintermsofbutter-flyfishcolonizing theRedSeaEightextant species fromCH4aredistributedinatleastsomepartsoftheRedSea(Chaetodon aurigaC fasciatus C leucopleura C lineolatus C melannotus C mesoleu‐cos C pictus and C semilarvatus)fourofwhicharerestrictedtotheArabianPeninsula(C fasciatus C mesoleucos C pictus and C semi‐larvatus) Moreover the reconstruction identified a mix of originstatesforCH4speciesfoundintheRedSeaBothC fasciatus andC leucopleurahavetheiroriginswithintheRedSeawhereasC lin‐eolatusandC mesoleucoshavetheiroriginsatSocotraTheoriginsofC semilarvatusareplacedinSouthOmanwhereastheoriginsofC pictusareplacedintheGulfofOmanWiththeexceptionofC lin‐eolatus awidespread Indo-West Pacific species all CH4 lineageshaveoriginsintheArabianPeninsularegionandIndianOceanandsubsequent dispersalwas limited from these sitesChaetodon lin‐eolatus appears to be the only species inCH4 to originate in theArabianPeninsulaandthendisperseacrossthebroaderIndo-WestPacificHoweverunsampledtaxafromthiscladearemorewidelydistributed across the Indian and POs (Supporting InformationFigureS2)
Threetaxaof thebannerfishcladearealsopresent in theRedSea (Heniochus diphreutes H intermedius Forcipiger flavissimus)withH intermediusconsideredaRedSeatoGulfofAdenendemicDespitethesetaxaonlybeingrepresentativeofasmallproportionoftheentirebannerfishcladethereconstructionsuggestsawide-spreadancestorthatdivergedintheArabianPeninsularegion(H in‐termedius)withsubsequent(successful)colonizationofthebroaderIndo-WestPacific(H diphreutesandF flavissimus)
TA B L E 2 emspAkaikeinformationcriterion(AIC)modeltestingbasedondistributionpatternsforbutterflyfishlineagesusingthetime-calibratedphylogenyanalyzedwiththeRmoduleBioGeoBEARSwheredrepresentsthedispersalparametererepresentstheextinctionparameterandjrepresentsfounder-eventspeciation
Ln likelihoodNumber of parameters d e j AIC AIC weight
DEC minus25513 2 006 0 0 51425 003
DEC+J minus25079 3 005 0 004 50758 076
DIVALIKE minus25388 2 007 004 0 51176 009
DIVALIKE+J minus25276 3 006 002 003 51152 011
BAYAREALIKE minus25986 2 005 018 0 52371 0
BAYAREALIKE+J minus25548 3 004 008 006 51696 001
Forthesemodelswecodedeachtaxonbasedonpresenceabsenceinninediscretegeographicalareas (A)GulfofAqaba (B)restofRedSea (C)DjiboutiandGulfofAden(D)Socotra(E)SouthOman(F)ArabianGulf(G)GulfofOmanandPakistan(H)restofIndianOceanand(I)PacificOceanBoldindicatesthefavoredmodelbasedonAICscores
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
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AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
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Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
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Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
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BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
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ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
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CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
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KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
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McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
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Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp11001DIBATTISTA eT Al
34emsp|emspCorrelational trait analysis evaluation of the ldquoecological traitrdquo hypothesis
Based on the best-fit PGLM depth range and phylogenetic agewerenegativelycorrelatedwithendemismwithdepthrangebeingastrongerpredictorthanphylogeneticage(Table3Figures5and6) Exploring these relationships using a regression tree approachreveals that theeffectofphylogeneticage isdependentondepthrangeEndemicspeciesfromtheArabianPeninsularegionarethere-foremore likelytobeyoungerthanwidespreadonesbutonlyforthose species with depth ranges extending to mesophotic reefs
(depthrangegt27mFigures5and6)Endemismwasnotcorrelatedwithanyoftheotherfactorsintheanalysisforthebutterflyfishesconsideredhere(SupportingInformationTablesS2andS4)
4emsp |emspDISCUSSION
Thisstudyused901 loci tosuccessfullygenerateagenome-scalephylogeny of bannerfishes and butterflyfishes endemic to thecoastal reefs of the Arabian Peninsula This is the first time thisgenomic method has been applied to species-level phylogenetic
F I G U R E 4 emspAncestralrangeestimationsinferredusingtheDEC+Jmodelbasedonatime-calibratedBayesianphylogenyofChaetodontidaespeciesStatesatbranchtipsindicatethecurrentgeographicaldistributionsoftaxawhereasstatesatnodesindicatetheinferredancestraldistributionsbeforespeciation(middle)andafter(corner)TheregionsconsideredinthisanalysisincludethefollowingGulfofAqabarestofRedSeaDjiboutiandGulfofAdenSocotraSouthOmanArabianGulfGulfofOmanandPakistanrestofIndianOceanandPacificOceanAbbreviationsPlio=PliocenePle=PleistoceneSignificantvicarianceintheRedSeatoArabianGulfregionisindicatedbyreddashedlines
Bannerfishes
Clade C
H2
Clade C
H3
Clade C
H4
Gulf of Aqaba
Red Sea
Dijibouti amp Gulf of Aden
Socotra
South Oman
Arabian Gulf
Gulf of Oman amp Pakistan
Indian Ocean
Pacific Ocean
Oligocene Miocene Plio Ple
30 25 20 15 10 5 0
A B C D E F G H I
Forcipiger longirostris
Forcipiger flavissimus
Heniochus intermedius
Heniochus diphreutes
Heniochus acuminatus
Chaetodon unimaculatus
Chaetodon kleinii
Chaetodon trichrous
Chaetodon madagaskariensis
Chaetodon mertensii
Chaetodon xanthurus
Chaetodon paucifasciatus
Chaetodon pelewensis
Chaetodon punctatofasciatus
Chaetodon guttatissimus
Chaetodon trifasciatus
Chaetodon lunulatus
Chaetodon austriacus
Chaetodon melapterus
Chaetodon larvatus
Chaetodon baronessa
Chaetodon triangulum
Chaetodon plebeius
Chaetodon speculum
Chaetodon zanzibarensis
Chaetodon bennetti
Chaetodon trifascialis
Chaetodon gardineri
Chaetodon leucopleura
Chaetodon melannotus
Chaetodon auripes
Chaetodon fasciatus
Chaetodon lunula
Chaetodon collare
Chaetodon oxycephalus
Chaetodon falcula
Chaetodon lineolatus
Chaetodon semilarvatus
Chaetodon mesoleucos
Chaetodon nigropunctatus
Chaetodon dialeucos
Chaetodon pictus
Chaetodon decussatus
Chaetodon vagabundus
Chaetodon auriga
Infilling of Arabian Gulf (~14 Ka)
Last Glacial Maximum (~18 Ka)
Closure of Red Sea connection to Mediterranean Sea
Formation of Strait of Bab al Mandab
Ma
ABCDEFGHI
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
AbererA JKobertKampStamatakisA (2014)ExaBayesMassivelyparallelBayesiantreeinferenceforthewhole-genomeeraMolecular Biology and Evolution 31 2553ndash2556 httpsdoiorg101093molbevmsu236
AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
Bejerano G Haussler D amp Blanchette M (2004) Into the heartof darkness Large-scale clustering of human non-coding DNABioinformatics20i40ndashi48httpsdoiorg101093bioinformaticsbth946
Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
11002emsp |emsp emspensp DIBATTISTA eT Al
analysesofareeffishgroupOurphylogenywhichincludesallshal-lowwater chaetodontid species found in theRedSea toArabianGulf and their close relatives distributed throughout the Indo-West Pacific provides divergence times with narrow confidenceintervals and biogeographic insight into this endemism hotspot
Reconstructingtheevolutionaryhistoryofthesefisheswiththeirwidespread relatives does not appear to support the evolution-ary incubator hypothesis That is despite generating significantbiodiversityintheformofendemicspeciestheseperipheralareasof theArabianPeninsula donot appear to have exported signifi-cantbiodiversity to thecentral Indo-WestPacific In factpoten-tiallyonlythreespecieswithreconstructedorigins intheArabianPeninsula (C lineolatusH diphreutes and F flavissimus) appear tosubsequentlydispersetotheIndo-WestPacificOurphylogeneticanalysesalsorevealedthatmostendemicspeciesoriginatedpriortoandpersisted through themajorenvironmental fluctuationsofthePleistocenewhichdoesnot support thePleistoceneextirpa-tionhypothesisTheecological trait-basedanalyses revealed thattheevolutionofRedSeatoArabianGulfendemicbutterflyfisheswasassociatedwithspecializationtoshallowreefhabitatandtoalesserextentspeciesrsquophylogeneticage
41emsp|emspEvaluation of the ldquoevolutionary incubatorrdquo hypothesis
TheRedSeaGulfofAdenArabianSeaandArabianGulfareallpe-ripheraltothebroaderIndo-WestPacificbiogeographicregionandpotentiallyproducecontributenewreef fishspecies to thecenter(seeBowen et al 2013Hodge et al 2014) Temporally theRedSea to ArabianGulf butterflyfish assemblage (17 species in total)is made up of recently diverged lineages with ages ranging from417Ma(F flavissimus)to116Ma(C austriacusC melapterussplit)InafewcasestheRedSeatoGulfofAdenendemicsappeartohavediverged as the earliest lineage of that clade (egC larvatus andC semilarvatusFigures2and3)Indeedtheldquooldestrdquoendemicbut-terflyfishlineageinourstudyC larvatus (286Ma43ndash16Ma95HPD)appearedinthelatePlioceneanddivergedfromanIndo-WestPacificlineagethatlatergaverisetospeciesallopatricbetweenthetwooceanbasins (C triangulum in the IndianOcean andC baron‐essainthePO)TheancestralrangereconstructionoftheseArabianPeninsulaendemicsdemonstratesconsistentcolonizationroutestothe Red Sea andArabian Sea via the IndianOcean from the east(Figure4)butwithfewexamplesofreciprocalexpansionfromthe
F I G U R E 6 emspTheclassificationofspecies-leveltraitsassociatedwithendemismamongtheRedSeatoArabianGulfbutterflyfishes(a)Dataontheleaves(representedbysquares)providetheprobabilityofendemism(top)andthepercentageofallobservationsinthenode(bottom)Therightpanelshowsthepredictionsurface(b)
Depth range gt27 m
Phylogenetic age gt175 Myr
027100
01160
044
04316
0540
Yes No
C austriacusC dialeucosC fasciatusC larvatusC melapterusC mesoleucosC nigropunctatusC pictusC semilarvatus
C gardineriC paucifasciatusH intermedius
Depth range
P
hylogenetic age
Prob of endemism
(a) (b)
TA B L E 3 emspSummaryofthefinal(best)phylogeneticlinearmulti-regressionmodelbasedonestimatedprobabilityofendemismasaresponsevariableselectedafterthebackwardstepwisephylostepprocedure
Estimate SE z value p value
(Intercept) 6170 2506 2461 0013
Depthrange minus1423 0543 minus2620 0008
Phylogeneticage minus1209 0694 minus1742 0061
Coefficientsinboldindicatesignificance(p lt 005)
F I G U R E 5 emspEstimatedprobabilityofendemismamongRedSeatoArabianGulfbutterflyfishspeciesincludingsomeoftheirclosestcongenersasafunctionofdepthrangeDifferentlinetypesrepresentvariabilityinestimatedspeciesphylogeneticageextractedfromFigurethinsp2(seelegend)
log Depth range (m)
Prob
abili
ty o
f end
emis
m
25 30 35 40 45 50
00
05
10
11 Myr16 Myr27 Myr45 Myr72 Myr
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
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AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
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Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
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ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
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DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
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HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
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RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
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RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
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SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
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sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
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SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp11003DIBATTISTA eT Al
ArabianPeninsulabacktothe IndianOceanandPOForexamplebothC larvatus andC semilarvatus appear to have historically di-vergedinDjiboutiGulfofAdenandSouthOmanrespectivelysuc-cessfullycolonizedtheRedSeabutnotestablishedfurthersouthandeastbasedonpresentdaydistributionsSimilarreconstructionresultswereobtainedfortheregionalendemicC pictus(RedSeatoGulfofOman)whichshowedapparenthistoricaldivergenceintheGulfofOmanandonlyrecentcolonizationofthesouthernlimitsoftheRedSea
OtherendemicsappeartohavehistoricallydivergedwithintheRedSea(C fasciatus)oradjacentDjiboutiandGulfofAden(C pauci‐fasciatus)butnotcolonizedanyfurthertothesoutheastAlthoughequivocalbasedontheprobabilisticuncertaintyofnodesinthean-cestralrangereconstructionofthemostlikelymodel(DEC+J)thereareanumberofcompetingexplanations forhowC austriacusandC melapterus diverged from each other within the coastal watersoftheArabianPeninsula(alsoseeWaldropetal2016)particularlysince C melapterus is the only species in this complex present intheArabianGulf Themost likely explanation is basedonpresentday distributions (Figure 3c) C austriacus is largely restricted tothenorthernandcentralRedSea(withrarerecordsinthesouthernRedSeaandoutsideoftheRedSea)whereasC melapterusismostabundantwithinoradjacenttotheArabianGulf(withrarerecordsin the southern Red Sea)mdashthese bodies of water show oppositetrendsintermsofproductivityseasurfacetemperatureandtem-poralpatternsofenvironmentalvariation (PousLazureampCarton2015Raitsosetal2013)Theseenvironmentalconditionsaread-ditionallysignificantlydifferentfromtherestofthe IndianOceanandthustheuniqueconditionsintheRedSeaandArabianGulfmayhelp explainhowendemics evolved or at least concentrated andpersistedintheseperipherallocations
Despite a lack of supporting evidence for the evolutionaryincubator hypothesis a clear pattern emerges that the uniqueenvironmentalconditionsintheseperipheralseasmayhavecon-tributed to the formationof endemic species asoutlined aboveFor example some butterflyfish subclades are comprised en-tirely of regional endemics (eg C dialeucos C mesoleucos andC nigropunctatus) which provides further evidence that coralreef habitat surrounding the Arabian Peninsula may have gen-erated a number of new taxaMoreoverC dialeucos anOmanispecies showsgeographical divergencewith the remaining taxainitsgroup(Figure3)whichallwentontocolonizetheRedSeaandtheArabianGulfandmusthavethereforeencounteredcon-trasting environments at the western and eastern margins oftheir rangeTheshallowArabianGulf started to fillwithseawa-terapproximately14000yearsagoafterbeingdryprior to thatduringthelastglacialmaximum(Lambeck1996)suggestingthatit was seeded by successivewaves of colonization from coastalOmanThesameprocesswouldhavebeenongoingat thewest-ernmargin of theC dialeucos range except that the conditionsencounteredintheRedSeawouldhavecontrastedtothoseintheArabian Gulf (DiBattista Choat et al 2016) So while there issomeevidence to suggestvicarianceat the scaleof theArabian
Peninsula (ie diversification ofmost taxa occurred in the Plio-Pleistocene)astrongerscenarioisthatnaturalselectiondrivenbythemajordifferencesinenvironmentandhabitatwithintheareaprobably played an important role in the formation of endemicspeciesassemblages(egGaitheretal2015)Thuseventhoughthedistributionofsomeof thebutterflyfishesconsidered in thepresentstudydoesstopabruptlyattheentranceoftheStraitofHormuz (Chaetodon collareC pictusandC gardneri) itdoesnotsupporttheargumentforgeographicallydrivenallopatryIndeedallof thesespecieshaveadifferentdistributional responseneartheotherendoftheirdistributionattheStraitofBabalMandabwhich includesstoppingbefore theStraitsorextending throughtheStraitsintothesouthernRedSea(Figure3)ThealternativeisthattheincumbentwidespreadbutterflyfishmayhaverestrictedtheRedSeatoArabianGulfendemicsfromexpandingfurtherviacompetitiveexclusion
ThecurrentenvironmentoftheRedSeaisspatiallystructuredwithmajorcontrastsinthecoololigotrophicwatersofthenorthernregioncompared to themuchhigher temperatures andproductivity of thesouthern region (ieFarasan Islands inSaudiArabia to theeastandDhalakArchipelagoinEritreatothewest)(Racaultetal2015Raitsoset al 2013) This shift in environmental conditions is most clearlydemonstrated in thedifferences in lifehistory traitsassociatedwithreeffishspeciesthatoccurinbothareasbutisalsoseeninabundanceestimates across these gradients (DiBattista Roberts et al 2016Robertsetal2016)Suchputativeselectiongradientsaremostevi-dentincoralswhichshowsignaturesoflocaladaptationtodivergentenvironmentalconditions(DrsquoAngeloetal2015)
42emsp|emspEvaluation of the ldquoPleistocene extirpationrdquo hypothesis
ThesecondhypothesisthatwetestedinthisstudywasthePleistoceneextirpation hypothesiswhich predicts that all Red Sea faunawereeliminated during the last glacial maxima (~18ka) and were onlyre-populatedvia recentcolonizationevents (seeBitonetal2008)The number of species diverging at early stages in the PleistocenedisputestheargumentthatRedSeafaunadidnotsurvivecompleteclosure or restriction ofwater flow at the Strait of Bab alMandab(Figure2)Althoughitclearlydoesnotcoincidewithasinglevicari-anceeventgiventhevariabilityinthesplittingdatesbetweencloselyrelated species (Figure 3 see Michonneau 2015 for invertebrateexamples)andancestralrangereconstructionfavoring+Jparametermodels(iefoundereventsbetweennon-adjacentoceanregionsseeTable2)glaciationslikelyplayedaroleintheirseparationMoreovereventhoughalmostall sisterspecieshavesmallareasofoverlapattheir rangeedgewhich isusually associatedwithallopatric specia-tioninourcasethesedonotcoincidewithgeographicalboundaries(ievicariantchokepoints)suchastheStraitofBabalMandab(seeFigure3Lambeck1996DiBattistaChoatetal2016)Infactthenon-congruentageanddistributionoftheendemicspeciesindicateaseriesofvariableeventswhichmayreflectlocalizedpatternsofhabi-tatandenvironmentalchangeasoutlinedinthepreviousDiscussion
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
R E FE R E N C E S
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AlfaroMEFairclothBCHarringtonRCSorensonLFriedmanM Thacker C E hellip Near T J (2018) Explosive diversifica-tion of marine fishes at the Cretaceous-Palaeogene boundaryNature Ecology amp Evolution2 688ndash696 httpsdoiorg101038s41559-018-0494-6
AllenGRSteeneRampAllenM(1998)A guide to angelfishes and but‐terflyfishes (250 pp)SydneyNSWOdysseyPublishing
Bailey G (2010) The Red Sea coastal landscapes and hominin dis-persals InThe evolution of human populations in Arabia (pp15ndash37)DordrechttheNetherlandsSpringer
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Bellwood D R Klanten S Cowman P F Pratchett M S KonowN amp van Herwerden L (2010) Evolutionary history of the but-terflyfishes (f Chaetodontidae) and the rise of coral feedingfishes Journal of Evolutionary Biology 23 335ndash349 httpsdoiorg101111j1420-9101200901904x
BianchiCNMorriCChiantoreMMontefalconeM ParraviciniVampRovereA(2012)MediterraneanSeabiodiversitybetweenthelegacyfromthepastandafutureofchangeInNStambler(Ed)Life in the Mediterranean Sea A look at habitat changes (pp 1ndash55)NewYorkNYNovaSciencePublishers
Biton E Gildor H amp PeltierW R (2008) Red Sea during the LastGlacial Maximum Implications for sea level reconstructionPaleoceanography23PA1214
BolgerAM LohseMampUsadel B (2014) TrimmomaticA flexibletrimmerforIlluminaSequenceDataBioinformatics302114ndash2120httpsdoiorg101093bioinformaticsbtu170
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BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
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ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
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CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
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sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
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SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
11004emsp |emsp emspensp DIBATTISTA eT Al
section The best example is the relatively young clade ofArabianPeninsulaendemicsC dialeucosC nigropunctatusandC mesoleucos (crownnodeage20Ma29ndash12Ma95HPD)ThisgroupappearstohavebeeninfluencedbyboundariespresentedbytheOmanicoast-line across areaswhere there are known changes in the upwellingregime(McIlwainClaereboudtAl-OufiZakiampGoddard2005ShiMorrisonBohmampManghnani2000)ThisisinsharpcontrasttotheIndo-West Pacific parrotfisheswhere present day species bounda-ries support the notion of allopatric divergence (Choat KlantenHerwerdenRobertsonampClements2012)andendemicsappeartohavediverged intooneormoresubsequentendemics (ie second-aryendemismRotondoSpringerScottampSchlanger1981)basedonsympatricallydistributedsister-speciespairs(highlightedinChoatetal2012)MoreoverRedSeaendemicsfrommostotherfamiliesofreeffishappeartohaveequalproportionsofallopatricallyandsympa-tricallydistributedsisterspecies(Hodgeetal2014)whichisnotthecaseforthebutterflyfishes
Thediversificationofthesebutterflyfishesoccurredatatimewhen the coral assemblages of the worldrsquos reefs underwent amajorchange incoralcompositionandgrowthformsTheglobalproportion of staghorn coral occurrences in coral assemblagespersistedthroughoutmostoftheCenozoicbutincreasedsubstan-tiallyduringthePlioceneandespeciallytheQuaternary(Renemaetal2016)Indeedtherapidlygrowingbranchingacroporidcor-alsoffereddifferentstructuralcomponentsintermsofshelterandfeedingforagingmodeswhencomparedtomassivecoralssuchasporitidsthatdominatedMiocenereefsmorethan5MaThusthechaetodontidsoftheArabianPeninsula(particularlythecorallivo-rousspecies)wereexposedtoamuchmoredynamicenvironmentthanthewidespreadIndo-WestPacificspecies(Coles2003)be-cause of their close associationwith sensitive coral genera thatproliferatedintheregion
43emsp|emspEvaluation of the ldquoecological traitrdquo hypothesis
Thethirdhypothesisthatwetesthere iswhetherecologicaltraitsare linked to the evolution of endemism among butterflyfishes intheRedSea toArabianGulfWe found a negative significant re-lationshipbetweenendemismanddepthrangeandtoalesserex-tent phylogenetic age for these butterflyfishes (Figures 5 and 6)The relationshipbetweenanarrowversusbroaddepth rangeandendemismsupportstheviewthatendemicspeciestendtobemorespecialized to local resources than widespread species (HawkinsRobertsampClark2000)Themajorityof regionalendemics in thisstudy had depth ranges that did not extend deeper than 25m(Figure6) despite the availability of light dependent coral habitatextendingbeyondthat(Kahngetal2010)Thebroadrangeofagesrepresentedbytheseshallowwaterspecialistssuggeststhatadap-tation to shallow reefs occurredmultiple times across a relativelywide time frame (ie13ndash33Myr)On theotherhand speciationofendemicswithapreferencefordeepreefsseemstobearecentphenomenonasdeeperdepthrangeswerestronglyassociatedwithyoungage(lt175MyrFigure6)
44emsp|emspComments on incomplete sampling and biogeographic biases
ThegoalofthisstudywastoreconstructtheevolutionaryhistoryofRedSeatoArabianGulfbutterflyfishesAsisthecasewithallphylogeneticandbiogeographicreconstructionsourresultshaveto be interpreted in light of the taxa that are not sampled bothextant and extinct Indeed the inclusion ofmissing taxa has thepotential to alter lineage relationships and their age estimateswhereas their geographic distribution may alter the most likelybiogeographicscenariosreconstructedacrossthetree(seediscus-sion inCowmanampBellwood 2013)Herewewere able to sam-pleallRedSea toArabianGulfbutterflyfishes (saveonespeciesR jayakari)andtheircloserelativesfromtheIndianOceanandPOacross fourmajor chaetodontid lineages (Supporting InformationFigure S2) From a temporal perspective the topology and agesestimated for thegenomic scaleUCEdataoverlapwithpreviousstudies(SupportingInformationFiguresS2andS3)Moreoveroursamplingofeight species thathavenotpreviouslybeen includedinphylogenetic studiesof theChaetodontidae familymeans thatfor 13 out of the 17 Arabian Peninsular species we are confi-dent thatwehavesampledtheirdirectsister lineageTwoof theoutstanding three species (C melannotus C trifascialis) arewide-rangingIndo-WestPacifictaxathatarereconstructedtohavedis-persed to theArabianPeninsula (Figure4)Themost likely sisterspecies ofC melannotus isC ocellicaudus (Kuiter 2002 also seeSupportingInformationFigureS2)awestPacificspeciesnotsam-pledinourdataset InthecaseofC trifascialis it isplacedasthesisterlineageforasubcladeofCH3containing10speciesdistrib-utedacross the IndianOceanandPOofwhichwesampled fourspecies (Supporting InformationFigureS2CowmanampBellwood2011)ThefinaloutstandingspeciesC leucopleura isplacedasasisterspeciestoC gardineriBothspecieshavenotpreviouslybeensampled inphylogeneticstudiesbutarerecognizedtobecloselyrelatedtoathirdspeciesChaetodon selene (widespreadinthewestPacificKuiter2002)whichwasnotsampledinourUCEdatasetIneachofthesethreecasesandmorebroadlyacrossthefamilythe inclusion of unsampled specieswould increase the influenceoftheIndianOceanandPOintheancestralestimationofbiogeo-graphicrangesAssuchitwouldacttostrengthenourconclusionthat even though the Red Sea and adjacent gulfs and seas havebeen importantforthegenerationofendemicspeciestheyhavehadlittlecontributiontothewiderIndo-WestPacificdiversityofbutterflyfishes
5emsp |emspCONCLUSION
Itappearsthattheuniqueenvironmentalconditions inthecoastalwatersoftheArabianPeninsulamayhavecontributedtotheforma-tionofendemicbutterflyfisheshoweverthereisalackofevidencefor endemics contributing significant species richness to adjacentseas (ieevolutionary incubatorhypothesis)Moreoverevenwith
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
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DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
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DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
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cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
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FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
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HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
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Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
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Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp11005DIBATTISTA eT Al
catastrophicenvironmental instabilityexperiencedbytheRedSeaandcoastalenvironmentsoftheArabianPeninsuladuetosealevelchangesassociatedwithglacialcycles(LudtampRocha2015)thereisnoevidenceforamassiveextirpationofbutterflyfishfauna intheregion(iePleistoceneextirpationhypothesisalsoseeDiBattistaChoatetal2016)Thebroadrangeofphylogeneticagesamongen-demicshallowwaterbutterflyfishessupportstheviewthatspeciesmayhavesurvivedinisolatedrefugiawithintheRedSea(DiBattistaChoat et al 2016) None of the dispersal-related traitswere as-sociatedwithendemism suggesting that factorsother than thoserelatedtospeciesintrinsicdispersalpotentialmaybelimitingdisper-salintothegreaterIndianOcean(egcoastlinegeographyoceano-graphicbarriers)
ACKNOWLEDG MENTS
This work was supported by the KAUST Office of CompetitiveResearch Funds under Award No CRG-1-2012-BER-002 andbaseline research funds toMLB National Geographic SocietyGrant 9024-11 to JDD National Science Foundation grantDEB-0842397 toMEA California Academy of Sciences fund-ing to LAR Australia Research Council Discovery ECR AwardDE170100516 to PFC For support in Socotrawe kindly thankthe Ministry of Water and Environment of Yemen staff at theEnvironment Protection Authority Socotra and especially SalahSaeed Ahmed Fouad Naseeb and Thabet Abdullah Khamis aswellasAhmedIssaAliAffrarfromSocotraSpecialistTourforhan-dling general logistics For logistic support elsewherewe thankEricMasonatDreamDiversNicolasPreacutevotatDolphinDiversandthe crew of theMVDeli in Djibouti David Pence the KAUSTCoastal and Marine Resources Core Lab and Amr Gusti theAdministrationof theBritish IndianOceanTerritoryandChagosConservation Trust theMinistry of Agriculture and Fisheries inOman including Abdul Karim theMinistegravere de la Pecircche et desReacutesources Halieutiques ndash Madagascar the Western AustraliaDepartmentofFisheriesParksAustraliaaswellastheUniversityofMilano-BicoccaMarineResearchandHighEducationCentreinMagoodhoo theMinistry of Fisheries andAgriculture RepublicofMaldivesandthecommunityofMaghoodhooFaafuAtollForspecimen collections we thank David Bellwood Brian BowenJohn Burns Darren Coker Richard Coleman Joshua CopusJoshuaDrewIriaFernandez-SilvaMichelleGaitherBrianGreeneElliott Jessup Randy Kosaki Jason Leonard Keo Lopes SarahLongo Cassie Lyons JenniferMcIlwain Gerrit Nanninga DavidPence Mark Priest Richard Pyle Freacutedeacuteric Ramahatratra MarkRoyer Pablo Saenz-Agudelo Anne Sheppard Charles SheppardJacquelineTrollerDanielWagnerRobertWhittonandmembersoftheReefEcologyLabatKAUSTForassistancewithbenchworkatKAUSTwe thankCraigMichellWe also acknowledge impor-tantcontributionsfromRobertJToonenJohnERandallJo-AnnCLeongandDavidCataniaforassistancewithspecimenarchiv-ingand theKAUSTBioscienceCoreLaboratorywithSivakumarNeelamegam and Hicham Mansour for their assistance with
IlluminasequencingSpecialthankstoScottPartridgefortheuseofhisillustrationsoftheChaetodontidaefamily
AUTHORSrsquo CONTRIBUTIONS
JDD MEA LAR JHC and MLB designed the studyJDDLSJPAHTHSLARandMLBcollectedsamplesJDD and LS generated theUCE libraries JDDMEA JCOJL and PFC analyzed and interpreted dataMF calibratedtreereconstructionsJDDwrotethemanuscriptwithinputfromallco-authors
DATA ACCE SSIBILIT Y
Data associated with this manuscript are available under NCBIBioProject PRJNA484421 available at httpswwwncbinlmnihgovbioprojectPRJNA484421
ORCID
Joseph D DiBattista httporcidorg0000-0002-5696-7574
Jonathan Chang httporcidorg0000-0002-3811-1254
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CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
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DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
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DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
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FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
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FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
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GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
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HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
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HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
11006emsp |emsp emspensp DIBATTISTA eT Al
BowenBWRochaLAToonenRJampKarlSA(2013)Theoriginsof tropicalmarine biodiversityTrends in Ecology and Evolution28359ndash366httpsdoiorg101016jtree201301018
CastresanaJ(2000)Selectionofconservedblocksfrommultiplealign-ments for their use inphylogenetic analysisMolecular Biology and Evolution17540ndash552httpsdoiorg101093oxfordjournalsmol-beva026334
Choat J H Klanten O S van Herwerden L Robertson D Ramp Clements K D (2012) Patterns and processes in the evo-lutionary history of parrotfishes (Family Labridae) Biological Journal of the Linnean Society 107 529ndash557 httpsdoiorg101111j1095-8312201201959x
ColeAJampPratchettMS (2014)Diversity indietandfeedingbe-haviourofbutterflyfishesRelianceonreefcoralsversusreefhabi-tatsInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp107ndash139)BocaRatonFLCRCPress
ColesSL(2003)CoralspeciesdiversityandenvironmentalfactorsintheArabianGulfandtheGulfofOmanAcomparisontotheIndo-PacificregionAtoll Research Bulletin5071ndash19
CowmanPF(2014)Historicalfactorsthathaveshapedtheevolutionof tropical reef fishesA reviewofphylogeniesbiogeographyandremainingquestionsFrontiers in Genetics51ndash15
Cowman P F amp Bellwood D R (2011) Coral reefs as drivers ofcladogenesisExpandingcoral reefscrypticextinctioneventsandthe development of biodiversity hotspots Journal of Evolutionary Biology242543ndash2562
CowmanPFampBellwoodDR(2013)ThehistoricalbiogeographyofcoralreeffishesGlobalpatternsoforiginationanddispersalJournal of Biogeography40209ndash224
CowmanPFParraviciniVKulbickiMampFloeterSR (2017)Thebiogeography of tropical reef fishes Endemism and provincial-ity through time Biological Reviews 92 2112ndash2130 httpsdoiorg101111brv12323
DAngeloCHumeBCCBurtJSmithEGAchterbergEPampWiedenmannJ(2015)Localadaptationconstrainsthedistributionpotential of heat-tolerant Symbiodinium from the PersianArabianGulf The ISME Journal 9 2551ndash2560 httpsdoiorg101038ismej201580
Dersquoath G amp Fabricius K E (2000) Classification and re-gression trees A powerful yet simple technique for eco-logical data analysis Ecology 81 3178ndash3192 httpsdoiorg1018900012-9658(2000)081[3178CARTAP]20CO2
DertiARothFPChurchGMampWuCT(2006)Mammalianultra-conservedelementsarestronglydepletedamongsegmentaldupli-cationsandcopynumbervariantsNature Genetics381216ndash1220httpsdoiorg101038ng1888
DiBattista JD BerumenM LGaitherM R Rocha L A Eble JA Choat J H hellip Bowen BW (2013) After continents divideComparative phylogeography of reef fishes from theRed Sea andIndianOcean Journal of Biogeography40 1170ndash1181 httpsdoiorg101111jbi12068
DiBattistaJDChoatJHGaitherMRHobbsJPLozano-CorteacutesDFMyersRFhellipBerumenML(2016)OntheoriginofendemicspeciesintheRedSeaJournal of Biogeography4313ndash30
DiBattistaJDGaitherMRHobbsJPASaenz-AgudeloPPiatekMJBowenBWhellipSinclair-TaylorTH(2017)Comparativephyloge-ographyofreeffishesfromtheGulfofAdentotheArabianSearevealstwocrypticlineagesCoral Reefs36625ndash638
DiBattistaJDRobertsMBouwmeesterJBowenBWCokerDFLozano-CorteacutesDFhellipBerumenML(2016)Areviewofcon-temporarypatternsofendemismforshallowwaterreeffaunaintheRed Sea Journal of Biogeography43423ndash439
DiBattista J D Wilcox C Craig M T Rocha L A amp Bowen BW (2010) Phylogeography of the Pacific Blueline SurgeonfishAcanthurus nigroris reveals high genetic connectivity and a
cryptic endemic species in the Hawaiian Archipelago Journal of Marine Biology2011httpsdoiorg1011552011839134
DosReisMampYangZ (2011)Approximate likelihoodcalculationonaphylogenyforBayesianestimationofdivergencetimesMolecular Biology and Evolution 28 2161ndash2172 httpsdoiorg101093molbevmsr045
EbleJAToonenRJSorensonLBaschLVPapastamatiouYPampBowenBW(2011)EscapingparadiseLarvalexportfromHawaiiinan Indo-Pacific reef fish theyellowtang (Zebrasoma flavescens)Marine Ecology Progress Series428245
FairclothBC(2013)illumiprocessorAtrimmomaticwrapperforparal-leladapterandqualitytrimminghttpsdoiorg106079J9ILL
FairclothBC(2016)PHYLUCEisasoftwarepackagefortheanalysisofconservedgenomiclociBioinformatics32786ndash788httpsdoiorg101093bioinformaticsbtv646
FairclothBCampGlennTC(2012)NotallsequencetagsarecreatedequalDesigningandvalidatingsequenceidentificationtagsrobusttoindelsPLOS ONE7e42543
Faircloth B C McCormack J E Crawford N G Harvey M GBrumfieldRTampGlennTC(2012)Ultraconservedelementsan-chor thousandsof geneticmarkers spanningmultiple evolutionarytimescalesSystematic Biology61(5)717ndash726
FairclothBCSorensonLSantiniFampAlfaroME(2013)Aphylog-enomicperspectiveontheradiationofray-finnedfishesbasedupontargetedsequencingofultraconservedelements(UCEs)PLOS ONE8e65923httpsdoiorg101371journalpone0065923
FesslerJLampWestneatMW(2007)Molecularphylogeneticsofthebutterflyfishes(Chaetodontidae)TaxonomyandbiogeographyofaglobalcoralreeffishfamilyMolecular Phylogenetics and Evolution4550ndash68
Froese R amp Pauly D (2011) FishBaseWorldWideWeb electronicpublicationRetrievedfromwwwfishbaseorg
GaitherMRBernalMAColemanRRBowenBWJonesSASimisonWBampRocha LA (2015)Genomic signaturesof geo-graphicisolationandnaturalselectionincoralreeffishesMolecular Ecology241543ndash1557httpsdoiorg101111mec13129
GaitherM R Jones S A Kelley CNewman S J Sorenson L ampBowenBW (2011)High connectivity in thedeepwater snapperPristipomoides filamentosus(Lutjanidae)acrosstheIndo-PacificwithisolationoftheHawaiianArchipelagoPLOS ONE6e28913httpsdoiorg101371journalpone0028913
GaitherMRToonenRJRobertsonDRPlanesSampBowenBW (2010) Genetic evaluation of marine biogeographical barriersPerspectives from twowidespread Indo-Pacific snappers (Lutjanus kasmiraandLutjanus fulvus)Journal of Biogeography37133ndash147
Girdler RWamp Styles P (1974) Two-stageRed Sea floor spreadingNature2477ndash11
GnirkeAMelnikovAMaguireJRogovPLeProustEMBrockmanWhellipRussC(2009)Solutionhybridselectionwithultra-longoli-gonucleotides for massively parallel targeted sequencing Nature Biotechnology27182ndash189
GrabherrMGHaasBJYassourMLevinJZThompsonDAAmitIhellipRegevA(2011)Full-lengthtranscriptomeassemblyfromRNA-seqdatawithoutareferencegenomeNature Biotechnology29644ndash652httpsdoiorg101038nbt1883
HarringtonRCFairclothBCEytanR ISmithWLNearTJAlfaroMEampFriedmanM (2016)Phylogenomicanalysisofca-rangimorphfishesrevealsflatfishasymmetryaroseinablinkoftheevolutionary eye BMC Evolutionary Biology 16 224 httpsdoiorg101186s12862-016-0786-x
HarrisRS(2007)ImprovedpairwisealignmentofgenomicDNAPhDThesisPennsylvaniaStateUniversity
HawkinsJPRobertsCMampClarkV(2000)Thethreatenedstatusof restricted-range coral reef fish speciesAnimal Conservation 381ndash88httpsdoiorg101111j1469-17952000tb00089x
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
emspensp emsp | emsp11007DIBATTISTA eT Al
HoLSTAneCLachlanRTarpinianKFeldmanRampHoMLST(2016)PackagelsquophylolmrsquoRetrievedfromftpvideolanc3slufprbrCRANwebpackagesphylolmphylolmpdf
HobbsJPAJonesGPMundayPLConnollySRampSrinivasanM(2012)Biogeographyandthestructureofcoralreeffishcommuni-tiesonisolatedislandsJournal of Biogeography39130ndash139httpsdoiorg101111j1365-2699201102576x
Hodge J RHerwerden L ampBellwoodD R (2014) Temporal evo-lutionofcoral reef fishesGlobalpatternsanddisparity in isolatedlocations Journal of Biogeography 41 2115ndash2127 httpsdoiorg101111jbi12356
Hsu K C Chen J P amp Shao K T (2007) Molecular phylogeny ofChaetodon (Teleostei Chaetodontidae) in the Indo-West PacificEvolution in geminate species pairs and species groups Raffles Bulletin of Zoology1477ndash86
Hubert-Ferrari A King G Manighetti I Armijo R Meyer B ampTapponnier P (2003) Long-term elasticity in the continental lith-ospheremodelling theAdenRidgepropagationand theAnatolianextrusion processGeophysical Journal International 153 111ndash132httpsdoiorg101046j1365-246X200301872x
Kahng S E Garcia-Sais J R SpaldingH L Brokovich EWagnerDWeil Ehellip Toonen R J (2010) Community ecology ofmeso-photiccoral reefecosystemsCoral Reefs29255ndash275httpsdoiorg101007s00338-010-0593-6
KatohKMisawaKKumaKampMiyataT (2002)MAFFTAnovelmethodforrapidmultiplesequencealignmentbasedonfastFouriertransform Nucleic Acids Research 30 3059ndash3066 httpsdoiorg101093nargkf436
KatohKampStandleyDM(2013)MAFFTmultiplesequencealignmentsoftware version 7 Improvements in performance and usabilityMolecular Biology and Evolution30772ndash780
KeithSAWoolseyESMadinJSByrneMampBairdAH(2015)Differential establishment potential of species predicts a shift incoralassemblagestructureacrossabiogeographicbarrierEcography381225ndash1234httpsdoiorg101111ecog01437
Kemp J (1998) Zoogeographyof the coral reef fishes of the SocotraArchipelago Journal of Biogeography 25 919ndash933 httpsdoiorg101046j1365-2699199800249x
KlausewitzW(1989)EvolutionaryhistoryandzoogeographyoftheRedSeaichthyofaunaFauna of Saudi Arabia10310ndash337
KuiterRH(2002)Butterflyfishes bannerfishes and their relatives A com‐prehensive guide to Chaetodontidae and MicrocanthidaeChorleywoodUKTMCPublishing
LambeckK(1996)ShorelinereconstructionsforthePersianGulfsincethe last glacial maximum Earth and Planetary Science Letters 14243ndash57httpsdoiorg1010160012-821X(96)00069-6
Lomolino M V (2005) Body size evolution in insular vertebratesGeneralityoftheislandruleJournal of Biogeography321683ndash1699httpsdoiorg101111j1365-2699200501314x
Ludt W B amp Rocha L A (2015) Shifting seas The impacts ofPleistocenesea-levelfluctuationsontheevolutionoftropicalmarinetaxaJournal of Biogeography4225ndash38
LuizOJAllenAPRobertsonDRFloeterSRKulbickiMVigliolaLhellipMadin JS (2013)Adultand larval traitsasdeterminantsofgeographic range size among tropical reef fishes Proceedings of National Academy of Sciences USA11016498ndash16502httpsdoiorg101073pnas1304074110
LuizOJMadinJSRobertsonDRRochaLAWirtzPampFloeterS R (2012) Ecological traits influencing range expansion acrosslargeoceanicdispersalbarriers InsightsfromtropicalAtlantic reeffishesProceedings of the Royal Society B279 1033ndash1040httpsdoiorg101098rspb20111525
MalayMCMDampPaulayG(2010)Peripatricspeciationdrivesdiver-sificationanddistributionalpatternofreefhermitcrabs(DecapodaDiogenidaeCalcinus)Evolution64634ndash662
MatzkeNJ(2013)ProbabilistichistoricalbiogeographyNewmodelsforfounder-eventspeciationimperfectdetectionandfossilsallowimproved accuracy andmodel-testing Frontiers in Biogeography4210
McCormackJEHarveyMGFairclothBCCrawfordNGGlennTCampBrumfieldRT(2013)Aphylogenyofbirdsbasedonover1500 locicollectedby targetenrichmentandhigh-throughputse-quencing PLOS ONE 8 e54848 httpsdoiorg101371journalpone0054848
McGeeMDFairclothBCBorsteinSRZhengJDarrinHulseyCWainwrightPCampAlfaroME(2016)ReplicateddivergenceincichlidradiationsmirrorsamajorvertebrateinnovationProceedings of the Royal Society B28320151413
McIlwainJLClaereboudtMRAl-OufiHSZakiSampGoddardJ S (2005) Spatial variation in age and growth of the kingfish(Scomberomorus commerson) in the coastalwatersof theSultanateofOmanFisheries Research73283ndash298httpsdoiorg101016jfishres200410020
McKinney M L (1997) Extinction vulnerability and selectivityCombining ecological and paleontological viewsAnnual Review of Ecology and Systematics 28 495ndash516 httpsdoiorg101146an-nurevecolsys281495
Michonneau F (2015) Cryptic and not-so-cryptic species in thecomplex ldquoholothuria (Thymiosycia) imaptiensrdquo (Forsskaringl 1775)(Echinodermata Holothuroidea Holothuriidae) Biorxiv 014225httpsdoiorg101101014225
Ottimofiore E Albouy C Leprieur F Descombes P Kulbicki MMouillot D hellip Pellissier L (2017) Responses of coral reef fishestopastclimatechangesarerelatedtolife-historytraitsEcology and Evolution71996ndash2005httpsdoiorg101002ece32800
PousSLazurePampCartonX(2015)Amodelofthegeneralcircula-tioninthePersianGulfandintheStraitofHormuzIntraseasonaltointerannualvariabilityContinental Shelf Research9455ndash70httpsdoiorg101016jcsr201412008
PratchettMS (2014)Feedingpreferencesanddietaryspecialisationamongobligatecoral-feedingbutterflyfishesInMSPratchettMLBerumenampBGKapoor(Eds)Biology of butterflyfishes(pp140ndash179)BocaRatonFLCRCPress
Racault M F Raitsos D E BerumenM L Brewin R J Platt TSathyendranath S amp Hoteit I (2015) Phytoplankton phenologyindices incoral reefecosystemsApplicationtoocean-colorobser-vationsintheRedSeaRemote Sensing of Environment160222ndash234httpsdoiorg101016jrse201501019
RaitsosDEPradhanYBrewinRJWStenchikovGampHoteit I(2013) Remote sensing the phytoplankton seasonal succession oftheRedSeaPLOS ONE8e64909httpsdoiorg101371journalpone0064909
RambautASuchardMAXieDampDrummondAJ(2014)Tracerv16RetrievedfromhttpsbeastbioedacukTracer
RenekerJLyonsEConantGChellipD (2012)Long identicalmulti-species elements in plant and animal genomes Proceedings of the National Academy of Sciences USA109E1183ndashE1191httpsdoiorg101073pnas1121356109
RenemaW Pandolfi JM KiesslingW Bosellini F R Klaus J SKorpantyChellipJohnsonKG(2016)ArecoralreefsvictimsoftheirownpastsuccessScience Advances2e1500850
RobertsMBJonesGPMcCormickMIMundayPLNealeSThorroldShellipBerumenML(2016)Homogeneityofcoralreefcom-munitiesacross8degreesoflatitudeintheSaudiArabianRedSeaMarine Pollution Bulletin 105 558ndash565 httpsdoiorg101016jmarpolbul201511024
RohlingEJGrantKBolshawMRobertsAPSiddallMHemlebenCampKuceraM(2009)AntarctictemperatureandglobalsealevelcloselycoupledoverthepastfiveglacialcyclesNature Geoscience2500ndash504httpsdoiorg101038ngeo557
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566
11008emsp |emsp emspensp DIBATTISTA eT Al
RotondoGMSpringerVGScottGAampSchlangerSO (1981)PlatemovementandislandintegrationmdashapossiblemechanismintheformationofendemicbiotaswithspecialreferencetotheHawaiianIslandsSystematic Biology3012ndash21
ShiWMorrisonJMBohmEampManghnaniV (2000)TheOmanupwellingzoneduring19931994and1995Deep‐Sea Research II471227ndash1247httpsdoiorg101016S0967-0645(99)00142-3
SiddallMRohlingEJAlmogi-LabinAHemlebenCMeischnerDSchmelzer IampSmeedDA (2003) Sea-level fluctuationsduringthelastglacialcycleNature423853ndash858httpsdoiorg101038nature01690
Siepel A Bejerano G Pedersen J S Hinrichs A S Hou MRosenbloom K hellip Haussler D (2005) Evolutionarily conservedelements invertebrate insectwormandyeastgenomesGenome Research151034ndash1050httpsdoiorg101101gr3715005
Simons C Pheasant M Makunin I V amp Mattick J S (2006)Transposon-freeregionsinmammaliangenomesGenome Research16164ndash172
Skillings D J Bird C E amp Toonen R J (2010) Gateways toHawailsquoi Genetic population structure of the tropical sea cucum-ber Holothuria atra Journal of Marine Biology 2011 httpsdoiorg1011552011783030
SmeedD (1997)SeasonalvariationoftheflowinthestraitofBahalMandabActa Oceanologica20773ndash781
SmithBTMcCormackJECuervoAMHickersonMJAleixoACadenaCDhellipBrumfieldRT(2014)Thedriversoftropicalspe-ciationNature515406ndash409httpsdoiorg101038nature13687
SunKMeiklejohnKAFairclothBCGlennTCBraunELampKimballRT (2014)Theevolutionofpeafowlandothertaxawithocelli(eyespots)AphylogenomicapproachProceedings of the Royal Society B28120140823httpsdoiorg101098rspb20140823
TalaveraGampCastresanaJ(2007)Improvementofphylogeniesafterremoving divergent and ambiguously aligned blocks from protein
sequence alignments Systematic Biology 56 564ndash577 httpsdoiorg10108010635150701472164
TherneauTAtkinsonBampRipleyB(2015)lsquorpartrsquoRpackageversion41-10
Waldrop E Hobbs J P A Randall J E DiBattista J D Rocha LAKosakiRKhellipBowenBW (2016)Phylogeographypopula-tionstructureandevolutionofcoral-eatingbutterflyfishes (FamilyChaetodontidae genus Chaetodon subgenus Corallochaetodon)Journal of Biogeography431116ndash1129
WhittakerRJampFernaacutendez-PalaciosJM(2007)Island biogeography Ecology evolution and conservationOxfordUKOxfordUniversityPress
Yabuta S amp Berumen M L (2013) Social structures and spawningbehaviour of Chaetodon butterflyfishes In M S Pratchett M LBerumenampBGKapoor(Eds)Biology of Butterflyfishes (pp200ndash225)BocaRatonFLCRCPress
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleDiBattistaJDAlfaroMESorensonLetalIceagesandbutterflyfishesPhylogenomicselucidatestheecologicalandevolutionaryhistoryofreeffishesinanendemismhotspotEcol Evol 2018810989ndash11008 httpsdoiorg101002ece34566