ice ages and butterflyfishes: phylogenomics elucidates the … · butterflyfishes and bannerfishes,...

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)


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)


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)


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


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


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 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 lineolatus 1


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 auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn


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 vagabundus

Chaetodon auriga

Chaetodon mesoleucos


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 madagaskariensis

Chaetodon mertensii

Chaetodon xanthurus

Chaetodon paucifasciatus


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


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


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


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


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







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI


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


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


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


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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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


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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


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


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









K E Y W O R D S













TAB

LE 1


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)


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



haet

odon

leuc

ople

uraC

haet

odon

mel

aptu

rusand

Chae

todo

n pi



pic

tus(andnotC

haet

odon

vag

abun


haet

odon

aus

tria

cusinthe


TAB

LE 1

emsp(Continued)





















3emsp |emspRESULTS











Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn

Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn





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 auriga



Chaetodon dialeucos


Chaetodon falcula



Chaetodon fasciatus

Chaetodon lunula

Chaetodon auripes

Chaetodon collare

Chaetodon gardineri



Chaetodon speculum


Chaetodon bennetti

Chaetodon plebeius


Chaetodon baronessa


Chaetodon larvatus



Chaetodon lunulatus



Chaetodon mertensii

Chaetodon xanthurus





Chaetodon kleinii

Chaetodon trichrous















Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4



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




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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S













































































































K E Y W O R D S













TAB

LE 1


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)


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



haet

odon

leuc

ople

uraC

haet

odon

mel

aptu

rusand

Chae

todo

n pi



pic

tus(andnotC

haet

odon

vag

abun


haet

odon

aus

tria

cusinthe


TAB

LE 1

emsp(Continued)





















3emsp |emspRESULTS











Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn

Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn





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 auriga



Chaetodon dialeucos


Chaetodon falcula



Chaetodon fasciatus

Chaetodon lunula

Chaetodon auripes

Chaetodon collare

Chaetodon gardineri



Chaetodon speculum


Chaetodon bennetti

Chaetodon plebeius


Chaetodon baronessa


Chaetodon larvatus



Chaetodon lunulatus



Chaetodon mertensii

Chaetodon xanthurus





Chaetodon kleinii

Chaetodon trichrous















Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4



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




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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S
















































































































TAB

LE 1


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)


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



haet

odon

leuc

ople

uraC

haet

odon

mel

aptu

rusand

Chae

todo

n pi



pic

tus(andnotC

haet

odon

vag

abun


haet

odon

aus

tria

cusinthe


TAB

LE 1

emsp(Continued)





















3emsp |emspRESULTS











Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn

Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn





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 auriga



Chaetodon dialeucos


Chaetodon falcula



Chaetodon fasciatus

Chaetodon lunula

Chaetodon auripes

Chaetodon collare

Chaetodon gardineri



Chaetodon speculum


Chaetodon bennetti

Chaetodon plebeius


Chaetodon baronessa


Chaetodon larvatus



Chaetodon lunulatus



Chaetodon mertensii

Chaetodon xanthurus





Chaetodon kleinii

Chaetodon trichrous















Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4



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




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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S






































































































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



haet

odon

leuc

ople

uraC

haet

odon

mel

aptu

rusand

Chae

todo

n pi



pic

tus(andnotC

haet

odon

vag

abun


haet

odon

aus

tria

cusinthe


TAB

LE 1

emsp(Continued)





















3emsp |emspRESULTS











Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn

Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn





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 auriga



Chaetodon dialeucos


Chaetodon falcula



Chaetodon fasciatus

Chaetodon lunula

Chaetodon auripes

Chaetodon collare

Chaetodon gardineri



Chaetodon speculum


Chaetodon bennetti

Chaetodon plebeius


Chaetodon baronessa


Chaetodon larvatus



Chaetodon lunulatus



Chaetodon mertensii

Chaetodon xanthurus





Chaetodon kleinii

Chaetodon trichrous















Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4



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




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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S

























































































































3emsp |emspRESULTS











Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn

Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn





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 auriga



Chaetodon dialeucos


Chaetodon falcula



Chaetodon fasciatus

Chaetodon lunula

Chaetodon auripes

Chaetodon collare

Chaetodon gardineri



Chaetodon speculum


Chaetodon bennetti

Chaetodon plebeius


Chaetodon baronessa


Chaetodon larvatus



Chaetodon lunulatus



Chaetodon mertensii

Chaetodon xanthurus





Chaetodon kleinii

Chaetodon trichrous















Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4



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




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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S










































































































Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn

Chaetodon pictus 2







Chaetodon auriga 1

Chaetodon auriga 2





Chaetodon m

esoleucos 2







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


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 za

nzibare

nsis 2

Chaeto

don zan

zibare

nsis





Chaetodon baronessa







Chaetodon lunulatus







Chaetodon m







Chaetodon trichrous


Chaetodon kleinii 2


Chaetod

on kleinii 1a

Chaetod

on kleinii 1

Clade CH2

Clad

e CH

3Clade CH4

Bannerfishes

Pomacanthus paru


Naso unicornis

Zanclus cornutus



Bothus pantherinus

Red S

ea to Arabian G

ul fIInnddiiiaaann

OOOOOccceeeaaaaannn


OOOOOccceeeaaaaannn





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 auriga



Chaetodon dialeucos


Chaetodon falcula



Chaetodon fasciatus

Chaetodon lunula

Chaetodon auripes

Chaetodon collare

Chaetodon gardineri



Chaetodon speculum


Chaetodon bennetti

Chaetodon plebeius


Chaetodon baronessa


Chaetodon larvatus



Chaetodon lunulatus



Chaetodon mertensii

Chaetodon xanthurus





Chaetodon kleinii

Chaetodon trichrous















Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4



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




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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S









































































































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 auriga



Chaetodon dialeucos


Chaetodon falcula



Chaetodon fasciatus

Chaetodon lunula

Chaetodon auripes

Chaetodon collare

Chaetodon gardineri



Chaetodon speculum


Chaetodon bennetti

Chaetodon plebeius


Chaetodon baronessa


Chaetodon larvatus



Chaetodon lunulatus



Chaetodon mertensii

Chaetodon xanthurus





Chaetodon kleinii

Chaetodon trichrous















Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4



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




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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S







































































































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




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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S








































































































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













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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S
















































































































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











Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S












































































































Bannerfishes

Clade C

H2

Clade C

H3

Clade C

H4

Gulf of Aqaba

Red Sea


Socotra

South Oman

Arabian Gulf


Indian Ocean

Pacific Ocean


30 25 20 15 10 5 0

A B C D E F G H I







Chaetodon kleinii

Chaetodon trichrous


Chaetodon mertensii

Chaetodon xanthurus






Chaetodon lunulatus



Chaetodon larvatus

Chaetodon baronessa


Chaetodon plebeius

Chaetodon speculum


Chaetodon bennetti


Chaetodon gardineri



Chaetodon auripes

Chaetodon fasciatus

Chaetodon lunula

Chaetodon collare


Chaetodon falcula





Chaetodon dialeucos

Chaetodon pictus



Chaetodon auriga





Ma

ABCDEFGHI







Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S











































































































Depth range gt27 m


027100

01160

044

04316

0540

Yes No



Depth range

P

hylogenetic age

Prob of endemism

(a) (b)



(Intercept) 6170 2506 2461 0013





log Depth range (m)

Prob

abili

ty o

f end

emis

m

25 30 35 40 45 50

00

05

10





















ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S
























































































































ACKNOWLEDG MENTS







ORCID



R E FE R E N C E S





































































































ice ages and butterflyfishes: phylogenomics elucidates the … · butterflyfishes and bannerfishes,...

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