genotyping by sequencing reveals contrasting patterns of ...€¦ · ecology and evolution....

Ecology and Evolution 20181ndash18 emsp|emsp1wwwecolevolorg

Received28March2018emsp |emsp Accepted29March2018DOI 101002ece34125

O R I G I N A L R E S E A R C H

Genotyping by sequencing reveals contrasting patterns of population structure ecologically mediated divergence and long- distance dispersal in North American palms

Anastasia Klimova12 emsp|emspAlfredo Ortega-Rubio1 emsp|emspDavid L J Vendrami2emsp|emsp Joseph I Hoffman2

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd

1CentrodeInvestigacionesBiologicasdelNoroesteSCLaPazBajaCaliforniaSurMexico2DepartmentofAnimalBehaviourBielefeldUniversityBielefeldGermany

CorrespondenceJosephIHoffmanDepartmentofAnimalBehaviourBielefeldUniversityBielefeldGermanyEmailjosephhoffmanuni-bielefelddeandAlfredoOrtega-RubioCentrodeInvestigacionesBiologicasdelNoroesteSCLaPazBajaCaliforniaSurMexicoEmailaortegacibnormx

Funding informationConsejoNacionaldeCienciayTecnologiacuteaGrantAwardNumber251919and280030

AbstractComparativestudiescanprovidepowerfulinsightsintoprocessesthataffectpopula-tiondivergenceandtherebyhelptoelucidatethemechanismsbywhichcontempo-rarypopulationsmay respond toenvironmental changeFurthermoreapproachessuchasgenotypingbysequencing(GBS)provideunprecedentedpowerforresolvinggeneticdifferencesamongspeciesandpopulationsWethereforeusedGBStopro-vide a genomewide perspective on the comparative population structure of twopalmgeneraWashingtonia and BraheaontheBajaCaliforniapeninsulaaregionofhighlandscapeandecologicalcomplexityFirstweusedphylogeneticanalysistoad-dresstaxonomicuncertaintiesamongfivecurrentlyrecognizedspeciesWeresolvedthreemaincladesthefirstcorrespondingtoW robusta and W filiferathesecondtoB brandegeei and B armataandthethirdtoB edulisfromGuadalupeIslandFocusingonthefirsttwocladeswethendelveddeeperbyinvestigatingtheunderlyingpopu-lationstructureStrikingdifferenceswerefoundwithGBSuncoveringfourdistinctWashingtoniapopulationsandidentifyingasuiteoflociassociatedwithtemperatureconsistentwithecologicallymediateddivergenceBycontrast individualmountainrangescouldberesolvedinBraheaandfewlociwereassociatedwithenvironmentalvariables implying amoreprominent role of neutral divergence Finally evidencewasfoundforlong-distancedispersaleventsinWashingtoniabutnotBraheainlinewithknowledgeofthedispersalmechanismsofthesepalmsincludingthepossibilityof human-mediateddispersalOverall our studydemonstrates thepowerofGBStogetherwithacomparativeapproach toelucidatemarkedlydifferentpatternsofgenomewidedivergencemediatedbymultipleeffectors

K E Y W O R D S

ArecaceaeBajaCaliforniapeninsulagenotypingbysequencing(GBS)human-mediateddispersalsinglenucleotidepolymorphism(SNP)

2emsp |emsp emspensp KLIMOVA et AL

1emsp |emspINTRODUC TION

Comparativephylogeographic studiesof codistributed species areof paramount importance in decoding how shared geological andecological histories may have affected contemporary species andpopulations (Papadopoulou amp Knowles 2016) By comparing thespatial genetic structure of multiple codistributed species com-parative studies allow the assessment of phylogeographical con-gruencewhich is a baseline for historical inference (Avise 2000GarrickRowellSimmonsHillisampSunnucks2008Hickersonetal2010HoffmanClarke LinseampPeck2011)Moreover a generalunderstanding of how species and populations responded to pastchallengesmightprovideuswithinsightsintohowpresentandfu-turehumanactivitieswillimpacttheplanetsbiota(AviseBowenampAyala2016)

Itisalsobecomingincreasinglyrecognizedthatinteractionsbe-tweenorganismsandtheirenvironmentcanshapethedistributionofspatialgeneticvariationandleadtolocaladaptation(AndersonWillisampMitchell-Olds2011)Thisinturnmayreducetheamountofgeneflowbetweenpopulationsultimatelyputtingthemonthepathto speciation (RundleampNosil 2005 Schluter 2000) Theprimarydifference between ecologically mediated divergence and neutraldivergenceisthattheformerresultsinapatternofisolationbyen-vironment (IBE) inwhichgenetic andenvironmental distances arepositivelycorrelatedindependentlyofgeographicdistance(ShaferampWolf2013WangampBradburd2014)Bycontrasttheneutraldiver-gencemodelemphasizestheroleofgeographicisolationinrestrict-ingtheexchangeofmigrantsbetweenpopulationswhichresultsinapatternofisolationbydistance(IBD)thatisfrequentlyobservedinnaturalpopulations(Prunieretal2017Wright1943)

Althoughspeciesthatsharethesamelandscapemayfacesimilarselective environments their capacity to adapt to these environ-mentsmaybespecies-orevenpopulation-specificandcandependon both extrinsic and intrinsic factors including the strength andnature of selection the amount of genetic diversity and the ex-tentofphenotypicplasticity (SorkGuggerChenampWerth2016)Consequentlyspeciesinhabitingacommonlandscapemayvaryintheircapacitytoadapttoecologicalgradientsandchangingenviron-mentsAssessingadaptiveresponsesamongrelatedspecieswithinsharedheterogeneous landscapesmaythushelpustounderstandpatternsofbiodiversityAmajorsteptowardthisgoalisidentifyingtowhat extent ecology gene flow and genomic architecture con-tributetowardvariability intheevolutionarypotentialofmultiple-relatedspecies inhabitingthesame landscape (Raeymaekersetal2017)

In this regard theBajaCaliforniapeninsulawith itsheteroge-neousarrayoflandscapesandhabitatsvaryingfromtropicaldecid-uousforestsandmesicoasestoxericdesertscrubmountainsandlowaltitudearidplainsisofparticularinterest(DolbyBennettLira-NoriegaWilderampMunguia-Vega2015)Thepeninsulawasformedaround5ndash10millionyearsago(mya)whentectonicforcesgaverisetotheGulfofCaliforniaandseparatedanarrowsectionoflandfromtheMexicanmainlandCurrentlyaseriesofmountainrangesmost

prominentlySierraSanPedroMartirSierraLibertadandSierraLaGigantaruninsuccessionalongthepeninsulafromnorthtosouthIthasbeensuggestedthattheupliftofthesemajorsierrasprobablybeganaround6ndash10myaandthattheirformationwastieddirectlytothesametectonicforcesthatopenedtheGulfofCaliforniaandcre-atedtheSanAndreasFaultsystem(Martiacuten-Barajas2014MuellerKier Rockwell amp Jones 2009) Together the sierras constitute amoreorlesscontinuousmountainousbackbonethatseparateseco-systemsslopingeastintotheGulfofCaliforniafromthoserunningwestwards into the Pacific and also creates a complex landscapegradientalongtheentirepeninsularthatisreflectedinaveryhighdiversityofenvironments (RiemannampEzcurra2007)Thisuniquenatural setup characterizedbyunusuallyhigh levelsofboth land-scapeandecologicalcomplexitycouldconceivablyshapethepopu-lationstructureofspeciesinhabitingthepeninsulaviabothneutralandecologicallymediatedprocesseswiththeirrelativeimportancedepending on intrinsic qualities of the species in question (Dolbyetal2015)

AnadditionaldimensionisprovidedbythemorerecenthistoryoftheBajaCaliforniapeninsulawhichexperiencedanotableeco-logicalshiftinvolvingprogressivearidificationaftertheLastGlacialMaximum(LindellNgoampMurphy2006RiddleHafnerAlexanderampJaeger2000)Drasticchangesinprecipitationacrossthepenin-sulaarebelievedtohaveledtoseveralendemicspeciesbecomingeither locally extinct or restricted to small isolated sites such asoases and canyons (Bernardi Ruiz-Campos amp Camarena-Rosales2007WehnckeLoacutepez-MedelliacutenampEzcurra2010)Thismajoreco-logical transition is thought to have most strongly affected spe-ciesdependentonfreshwatersuchasamphibians(Grismer2002)fishes(Bernardietal2007)andmanyplants(LeoacutendelaLuz2014WehnckeampLoacutepez-Medelliacuten2014)However thesessilenatureofplantsrendersthemparticularlysusceptibletotheinfluenceoffine-scaleenvironmentalheterogeneity(Sorketal2016)whichmakesthefloraoftheBajapeninsulaideallysuitedtoexploringtherelativecontributionsofgeographyandecologytowardspecies-specificre-sponsestoaridification

Palms (Arecaceae)areaspecies-rich taxonomicgroupthathaslongbeenconsideredamodelplantfamilyforevolutionaryandeco-logicalstudiesinthetropics(Baconetal2016CouvreurampBaker2013Kisslingetal2012Savolainenetal2006)Althoughpalmsmainlyoccur in tropical andsubtropical climates (TregearRivalampPintaud 2011) a few species can alsobe found in desert regions(Dransfield etal 2008 Tomlinson 2006) Palm populations onthe Baja California peninsula are widely considered to be relictsof historically more widespread and continuous populations thatare now largely confined to sites where permanent water existseitheraboveorbelowtheground(Axelrod1958BaconBakerampSimmons2012Cornett1985abCornettGlenampStewart1986Felgeramp Joyal 1999GrismerampMcGuire 1993) This is reflectedby the fossil recordwhichshowsthatduring the lateCretaceouspalmswerecommonacrossNorthAmericaandextendedmuchfur-therthantheircurrentgeographicdistribution(CouvreurForestampBaker2011Harley2006)Todaytheonlysuitablenaturalhabitats

emspensp emsp | emsp3KLIMOVA et AL

fortropicalspecies likepalmsontheBajaCaliforniapeninsulacanbe found in small isolated pockets at the bottoms of canyons oroasesthatareseparatedbyacontinuousexpanseofmountainousdesertsandxericshrubland(Grismer2000HafnerampRiddle2011Minnich Franco-Vizcaiacuteno amp Salazar-Cesentildea 2011 Wehncke ampLoacutepez-Medelliacuten2014)

OntheBajapeninsulatheArecaceaeisrepresentedbytwonativeNorthAmerican palm generaWashingtonia and Brahea (GarcillaacutenVegaampMartorell2012Minnichetal2011) Washingtoniaisrepre-sentedbytwospeciesW robusta and W filiferaalthoughingeneraltaxonomic relationships within this genus remain poorly resolved(FelgerampBroyles2007FelgerampJoyal1999HendersonGaleanoamp Bernal 1995 McClintock 1978) as they are mainly based onmorphologicalcharacterssuchassizeleafshapeandinflorescencestructureW robustaismoreabundantonthesouthernpartofthepeninsulawhileW filiferamainlyoccupies thenorthernpeninsulaaswellassoutheasternCalifornia(Minnichetal2011)W robusta isalsofoundinafewripariancanyonsatthesouthernedgeoftheSonoranDesertontheMexicanmainland(FelgerampJoyal1999)

The Brahea complex comprisesnine species twoofwhichareendemicandrestrictedtotheBajaCaliforniapeninsula (B brande-geei and B armata) and one (B edulis) toGuadalupe Islandwhichlies 260km off the Pacific coast of the peninsula (Garcillaacuten etal2012Moran1996Oberbauer2005)Braheaisarguablytheleaststudied genusofAmericanpalms and consequently relationshipsbetween and within Brahea species have not been clearly de-scribed(Hendersonetal1995Minnichetal2011Quero1992)Nevertheless B brandegeei has been described as occupying thesouthernhalfoftheBajaCaliforniapeninsulafromSierraLaLagunaatthesouthernmosttipofthepeninsulatoSierraSanFranciscointhenorthernBajaCaliforniaSur (FelgerJohnsonampWilson2001Minnich etal 2011) while B armata has been described as ex-tendingnorthwardsfromthestatelineofBajaCaliforniaSurinthecentralpeninsulatojustsouthoftheUnitedStatesndashMexicoborder(Franco-VizcaiacutenoLoacutepez-BeltraacutenampSalazar-Cesentildea2007Wiggins1980)HowevertheexactdistributionallimitsofB brandegeei and B armataremainsomewhatunclearduetotaxonomicuncertainties(Felgeramp Joyal 1999 Felger etal 2001Hendersonetal 1995)FinallyB edulisisanendemicspeciesfounduniquelyonGuadalupeIsland (29degN 118degW) a seven-million-year-old volcanic island lo-cated260kmwestof theBajaCaliforniapeninsula (Batiza1977)ItisgenerallybelievedthatGuadalupeIslandhasneverbeenincon-tactwitheithertheMexicanmainlandortheBajapeninsulawhichwouldimplythatBraheapalmscolonizedtheislandvialong-distancedispersalCurrentlythesepalmsmainlyoccupyasmallareaoffogoasis in the far northern part of the Island (Garcillaacuten etal 2012LeoacutendelaLuzRebmanampOberbauer2003Oberbauer2005)

From an ecological perspective palm populations of the Bajapeninsula generally form small local colonies or elongate galler-ieswith plants growing almost entirely in areaswith supplemen-talwaterthatisinclosevicinitytospringsoralongwatercourses(Franco-Vizcaiacutenoetal2007Minnichetal2011)Washingtonia and Brahea co-occur along the slopesofmostof the sierras including

SierraJuarezSierraAsambleaSierraMechudoandSierraLaLaguna(KlimovaHoffmanGutierrez-RiveraLeondelaLuzampOrtega-Rubio2017Minnichetal2011)Howevertheydiffersomewhatintheirecologicalrequirementswiththeirestimatednicheoverlaprangingfromaround05ndash07dependingonthestatisticused(Klimovaetal2017)InparticularWashingtoniapalmshavestricterecologicalre-quirementsthanBraheapalmsandthereforeoccupyasmallertotalarea of the Baja California peninsula (Minnich etal 2011) Theyaremost commonly found at low-elevation oaseswherewater isrelativelyplentifulandtemperatures tendtobewarmerandmorestableBycontrastBraheapalmsarecapableoftoleratingdriercon-ditionsandthusoccupyamuchwiderelevationalrangeAccordinglyW filifera and W robustaareseldomfoundabove1000mwhereasB armatamaygrowatelevationsashighas1400mintheSierraSanPedroMartirandB brandegeeioccursatuptoaround1700mintheSierraLaLaguna(Minnichetal2011)

Species-specific modes and patterns of dispersal are anotherkeydeterminantofgeneticstructure intheArecaceae (EiserhardtSvenning Kissling amp Balslev 2011) Although vertebrates suchasbirds bats coyotes and foxeshavebeenproposedaspossibleseeddispersalagentsforbothWashingtonia and Braheatheeffectof these agents on the population structure and genetic diversityofpalmshasnotbeenevaluated(Cornett2008Silverstein2005)Furthermore recent studies of Brahea palms suggest that waterpulsesmaybe farmoresignificant in termsofseeddispersal thanbirds and small mammals (Wehncke Loacutepez-Medelliacuten amp Ezcurra2009Wehnckeetal2010)Thisleadstothepredictionthatdisper-sal in Braheapalmsshouldoccurmainlywithinwatercoursesorcan-yonsandhencethatconnectivityamongsierraswillberestrictedAfurthercomplicationisthepotential influenceofhumanswhichispredictedtobestrongerforWashingtoniaasthisgenusiswidelyconsideredtohavebeenfavoredbyindigenouspeopleoverBrahea asanimportantsourceofbothfoodandbuildingmaterials(FelgerampJoyal1999FelgerampMoser1985Minnichetal2011)

For the reasons described above Washingtonia and Brahea palmsprovide an attractive system for investigating the contribu-tions of neutral non-neutral and human-mediated effects towardpopulation structure in a comparative context However despitetheemblematicstatusofthesedesertpalmsmanyaspectsoftheirtaxonomy remain ambiguous (Minnich etal 2011) This is partlybecausepreviousgenetic studiesdonot always support currentlyrecognizedspeciesForexampleBaconetal(2012)didnotfindanyevidenceinsupportofthedesignationofW robusta and W filifera asseparatespeciesbasedonthreeplastidandthreenucleargenesThisambiguityistosomeextentreflectedbyamorerecentstudyofWashingtonia and Brahea palms from theBajaCaliforniapeninsulaandadjacentareasagainbasedonnuclearandchloroplastsequencedata(Klimovaetal2017)HerebothgenerawerefoundtoexhibitlowgeneticdiversityandminimalstructuringwithinthepeninsulasimilarlytopreviouslyreportedforW filiferainasmallregionoftheCalifornianmainlandusingallozymes(McClenaghanampBeauchamp1986)HoweverW filifera could be distinguished fromW robusta basedon chloroplast but not nuclearDNAwhereasB edulis was


divergent from its peninsular sister species based on nuclear butnot chloroplastDNA Such incongruences togetherwith the gen-erally lowgenetic resolutionprovidedby themarkersused in thisstudyprecludedcomprehensivehypothesistestingandthusmoredetailed inferencescouldnotbemadeConsequentlyat thepres-enttimeeventhegeographiclimitsoftheWashingtonia and Brahea species present on the Baja California peninsula remain unclear(Hendersonetal1995Klimovaetal2017Minnichetal2011)whilevirtuallynothingisknownaboutrelationshipsamongpopula-tionsfromdifferentsierras

Studiesbasedononeorhandfulofgenes like thosedescribedabovemayalsosufferfromanumberofbiasesrelatedtostochas-ticprocesses(HeathHedtkeampHillis2008Moore1995RokasampCarroll 2005)However approaches capable of genotyping thou-sandsofsinglenucleotidepolymorphisms(SNPs)suchasgenotypingbysequencing(GBS)arecapableofprovidingmuchgreatercoverageofthegenome(DeDonatoPetersMitchellHussainampImumorin2013Elshireetal2011)Recentsimulationandempiricalstudiessuggest that these approaches shouldbe superior to ahandful ofmarkers at capturing variation in drift selection recombinationandmutation(MorinLuikartampWayne2004)andtherebyprovidea more accurate depiction of population differentiation (SpinksThomsonampShaffer2014Vendramietal2017)andgeneticdiver-sity(Fischeretal2017Hoffmanetal2014)

ToaddresstheissuesdescribedabovewecombinedGBSwithnear-exhaustivesamplingofallfivenativeWashingtonia and Brahea palmspeciespresentontheBajaCaliforniapeninsulaandGuadalupeIslandThe resultingdatawere thenanalyzedon two levelsFirstweattemptedtoresolvetaxonomicrelationshipsandfromtheretodelimitthegeographicboundariesofeachspeciesonthepeninsulaSecondwefocusedwithinthemajorcladesidentifiedbytheformeranalysisandconductedpopulationgeneticanalysestouncoverpat-ternsofpopulationstructureontheBajapeninsulaandinvestigate

thepotentialunderlyingdriversOurmainworkinghypotheseswereasfollows(1)WeexpectedtofindgenomicsupportformostifnotallofthecurrentlyrecognizedspecieswiththepossibleexceptionofW robusta and W filifera(2)aswaterpulsesappeartobeanimport-antmediatorofdispersalinBraheapalmswehypothesizedforthisgenusthatdispersalwouldbemainlyrestrictedwithinwatershedswhich should be reflected in stronger population structure thanin Washingtonia and potentially manifested in a pattern wherebyeachsierraisgeneticallydistinct (3)wehypothesizedthatecolog-icallymediatedselectionshouldbecomparablymore important inWashingtonia palms due to their stricter ecological requirementswhichcouldpotentiallyleadtoanIBEpatternBycontrastweex-pectedBraheapalmstobemoreinfluencedbyneutralprocessesandthustoexhibitanIBDpattern(4)finallyduetothelonghistoricalassociationbetweenWashingtoniapalmsandhumanswehypothe-sizedthatpopulationstructureinWashingtoniacouldpotentiallyalsohavebeeninfluencedbyhuman-mediatedtranslocationevents

2emsp |emspMATERIAL S AND METHODS

21emsp|emspSample collection

Wecollecteda totalof190 leaf samples fromall fivepalmspe-ciesnativetotheBajaCaliforniapeninsulaandGuadalupeIsland(Figure1TableS1)Oursamplesizereflectsthedifficultyofcol-lectingsamplesfromendemicsthatarelocallyrareandcanonlybefoundatsmallandisolatedstandsthatcanoftenonlybereachedbyfootWecollectedspecimensfromvirtuallyallaccessibleoasesduring two consecutive field seasons each lasting ~4weeksWhenever possible we avoided sampling immediately adjacentindividualsasMiglioreetal(2013)showedthataroundathirdofadjacentsampledindividualsofarelictshrubspecieswereclonesFor comparisonwealso included twopopulationsofW robusta

F IGURE 1emspMapsshowingtheoases(points)andthesierras(shapefiles)fromwhich(a)Washingtoniaand(b)Brahea palmsweresampledThefullnamesoftheoasesandsamplesizesaregiveninTableS1Thecolorsoftheshapefilescorrespondtospecies(asdefinedinMinnichetal2011)(a)W robusta on theBajapeninsulaandMexicanmainlandand W filiferaatSJ(b)B edulisattheGuadalupeIsland(GI)B armataatSL SA CAT SSPM and SJ and B brandegeeiatSLL SM SPP and SSF

(a) (b)


from Sonora on theMexicanmainlandWewere therefore ableto cover the full distributional ranges of three Brahea species(B edulis B armata and B brandegeei)andoneWashingtoniaspe-cies (W robusta)whileW filifera couldonlybe sampled from itssouthern distributional limit in Sierra Juarez Mexico (Figure1TableS1)Specimenswereassignedtotaxabasedonspeciesdis-tributionsgivenbyMinnichetal (2011)Withinspeciespopula-tionswere defined based on the sierra fromwhich the sampleswerecollectedForWashingtoniawespecifiedeightpopulationscorrespondingtopalmsfrom(1)SierraLaLaguna(SLL) (2)SierraMechudo(SM) (3)SierraGiganta(SG) (4)SierraSanPedro(SSP)(5)SierraSanFranciscocombinedwithSierraLibertad (SFSL) (6)Catavintildea (CAT) (7) Sierra Juarez (SJ) and (8)MexicanmainlandstateofSonora(SON)ForBraheawespecifiedninepopulationsontheBajapeninsulacorrespondingto(1)SierraLaLaguna(SLL)(2)SierraMechudo(SM)(3)SierraSanPedro(SSP)(4)SierraSanFrancisco(SSF)(5)SierraLibertad(SL)(6)SierraAsamblea(SA)(7)Catavintildea(CAT) (8)SierraSanPedroMartir (SSPM)and(9)SierraJuarez(SJ)(Figure1TableS1)

22emsp|emspGenetic analysis

Total genomic DNA was extracted from silica-dried leaves usinga modified CTAB protocol (Gutierrez-Rivera in preparation) and50 μl ofDNA from each samplewas sent to theCornell InstituteofGenomicDiversityforlibrarypreparationandGBS(Elshireetal2011)EachDNAextractwasdigestedusingtherestrictionenzymePstI and subsequently a sample-specific barcoded adapter and acommon adapterwere ligated to the sticky ends of fragments toallow for sample discrimination after pooling A unique barcodedadapterwasusedforeachsampleplustwonegativecontrolsgivingatotalof192barcodesemployedNextsamplesfromthetwodif-ferentgenerawerepooledtogetherintotwoseparatelibrariesthatwereeach100bpsingle-endsequencedononelaneofanIlluminaHiSeq2000

The resulting raw readswereprocessedusing theTASSEL30pipeline (Bradbury etal 2007)which implements the customizedworkflowspecificallydesignedforGBSdatadescribedbyGlaubitzetal(2014)Specificallyallidenticalreadswerefirstcollapsedintotagsandthenumberof readsusedfor thegenerationofeachtagwasreportedBeforethisstepinordertoensuretheusageofexclu-sivelyhigh-qualityreadsonlyreadscontainingabarcodethecor-rectrestrictionenzymecuttingsiteandwithnoNswereretainedAfter removing thebarcode sequences the remaining readswerethentrimmedtoafinallengthof64bpwithanyreadscontainingasecondrestrictionsitebeingtruncatedThenaldquomasterrdquolistoftagswascreatedcontainingonlytagsbuiltfromatleastthreereads(ietheminimumdepthofcoverageofataghadtobethreereads)Thisnumber was chosen because lower values will result in more se-quencingerrorsbeingincludedwhilehighervalueswillresultintheexclusionofrareallelesWealsochoseavalueofthreebecausethisallowedtagscontaininguptothreesequencingerrorstobeassem-bledwhichincreasedthedepthofcoverageofnon-errorpositions

SequencingerrorsweresubsequentlyremovedbyfilteringoutSNPswithlowminorallelefrequencies(MAF)asdescribedbelow

Finally the master list of tags was aligned to the date palm(Phoenix dactylifera)referencegenome(datepalmdownloadedfromhttpswwwncbinlmnihgovgenome in June 2016) using thesoftwareBWA(LiampDurbin2009)toproduceaSAMfileAftercon-versionof this filewithSAMConvertor the tbt2vcfplug-inwithinTASSEL30wasusedtocallSNPsfromtagsthatalignedtouniquelocationsinthereferencegenomewhichwerethenexportedinVCFformatSNPswithMAFbelowthan001werethenremovedfromthedatasetinordertofilteroutfalseSNPsoriginatingfromsequenc-ingerrorswhileretaininggenuinevariantsincludingmoderatelyrarealleles InDelswerethenremovedfromthevariantdatasetwhichwas further filtered todiscard chloroplast andmitochondrial vari-antsSNPsthatwerenotbi-allelicandlocicarryingonlyheterozy-gotegenotypeswhichrepresentputativelyparalogouslociNextinordertoavoidlinkagebetweenlociweprunedtheSNPsforlinkagedisequilibrium using the thinning option in VCFTOOLS (Daneceketal2011)witha5kslidingwindowFinallyweremovedlociwithmorethan20missinggenotypesThisconservativemeasurewastaken tominimize the frequencyofgapsand thereby tomaximizetherobustnessofourdownstreamanalysesThefinaldatasetwasusedforphylogeneticanalysisandtocomparelevelsofgeneticdi-versitybetweenthetwogeneraAfterthatwegeneratedtwosep-arate datasets forWashingtonia and Brahea respectively to allowfiner-scalepopulationgeneticanalysesThesedatasetsweregener-atedforeachgenususingthesamefilteringstepsdescribedaboveAdditionallyfiveindividualswithmorethan30missingdata(fourWashingtonia and one Brahea)wereexcludedfromfurtheranalysesManipulationsoftheVCFfileswerecarriedoutusingVCFTOOLSInbreeding coefficients and observed and expected heterozygosi-tieswerecalculatedforeachpalmgenusseparatelyusingPLINK19(Changetal2015)

23emsp|emspComparative phylogenetic analyses

Inordertoresolvetaxonomicrelationshipsamongthemorphologi-callydefinedspeciesandtodelimitthegeographicboundariesofeachspeciesweperformedBayesianphylogeneticreconstructionusingtheSNAPPpackage(BryantBouckaertFelsensteinRosenbergampChoudhury 2012) within the program BEAST2 (Bouckaert etal2014)Duetocomputationallimitationswewereunabletoanalyzethe full dataset and therefore restrictedour analysis to a randomselectionofthreeindividualsperpopulationresultinginatotalof54 individualsrepresentingtwopalmgeneraWeusedthedefaultpriorandmodelparametersincludingthedefaultsforuandv(thebackwardandforwardmutationratesrespectively)andranasingleMarkovchainMonteCarlo (MCMC)chainof2000000 iterationswithsamplingevery1000stepsAfterrunningthefulldatasetwethenanalyzedeachgenusseparatelyusingsameparametersasbe-foreAcceptablemixing(requiringeffectivesamplesizevaluestobeat least 200) and convergencewere checked by visual inspectionof theposteriorsamplesusingTRACER(RambautSuchardXieamp


Drummond2014)Weusedaburn-inof10andvisualizedthedis-tributionoftreesusingDENSITREE21(Bouckaert2010)

24emsp|emspPopulation structure analyses

Based on the results of phylogenetic analyses (see Section3)wedecidedtoexcludeB edulisfrompopulation-levelanalysesorwhereappropriate to use it as an outgroupDownstreampopulation ge-netic analyses were conducted after defining samples from eachofthesierrasasa prioripopulations(Figure1TableS1)Firstpair-wise Fst values among sierraswere calculatedwithin theprogramGENODIVE(MeirmansampVanTienderen2004)withstatisticalsig-nificancedeterminedonthebasisof10000permutationsThenweusedsNMF12 (FrichotMathieuTrouillonBouchardampFranccedilois2014)toestimateindividualadmixturecoefficientsandtodeterminethemostprobablenumberofgeneticclusters(k)presentwithineachgenussNMFwaschoseninpreferencetomorecomputer-intensiveapproachessuchasSTRUCTURE(PritchardStephensampDonnelly2000)as ituses fastandefficientsparsenon-negativematrix fac-torization algorithms that considerably reduce the computationalburden without any appreciable loss of accuracy (Frichot etal2014 PopescuHarper Trick Bancroft ampHuber 2014Wollsteinamp Lao 2015) The best k valuewas inferred by calculating cross-entropyvaluesfrommultiplerunswithksetbetweenoneandtenRobustnessoftheresultswasassessedbyrunningfivereplicatesforthebestvalueofkusinganalpharegularizationparameterof100Weconductedmodelaveragingof individualancestrycoefficientsacross replicates and calculated the average pairwise similarity ofindividual assignments across runs using CLUMPP (Jakobsson ampRosenberg2007)FinallyweconvertedtheSNPdataintoamatrixofindividualpairwisegeneticdistancesusingtheRpackageSTAMPP(PembletonCoganampForster2013)andgeneratedaphylogeneticnetwork using the NEIGHBORNET algorithm (Bryant ampMoulton2004)withinSPLITSTREE4144(HusonampBryant2006)

25emsp|emspPopulation splits and migration modeling

WeusedtheapproachofPickrellandPritchard(2012)toinferthepopulationhistoryof thepalm taxausinggenome-wideallele fre-quencydataasimplementedinTREEMIX112(PickrellampPritchard2012) TREEMIX infers gene flow between populations by simul-taneously analyzingpopulationdivergenceandadmixtureOn theresultingmaximum-likelihood (ML) treemigration events are rep-resented by edges that connect populations via admixture SNPdata forWashingtonia and Brahea were converted from a diploidgenotype format into population-level allele counts using the py-thonscriptplink2treemixpy(availablewithTREEMIX)Eachpopula-tionwasrepresentedbyindividualsfromagivensierraasdescribedpreviouslyForWashingtoniaweusedthemostdivergentsierra(SJ)asanoutgroupwhileforBraheaweusedB edulisasanoutgroupWe first generated a maximum-likelihood graph with no migra-tioneventsbasedon1000bootstrap replicatesThenwe testedforbetweenoneandtenmigrationeventspertaxon(m1ndashm10)and

performedlikelihoodratioteststoallowstepwisecomparisonoflog-likelihoodvaluesbetweeneachpairofmigrationeventsAfterthatweformallytestedforadmixtureusingtheldquothree-populationtestrdquo(Pattersonetal 2012) implemented inTREEMIXThis is a formaltestthatcanprovideevidenceofadmixtureeveninthepresenceofpastmigrationevents(Pattersonetal2012)ItallowsdetectionofthepresenceofadmixtureinpopulationXfromothertwopopula-tionsAandBifthevalueoff3(XAB)isnegativethenthedevia-tionfromldquotreenessrdquoisdetectedandXappearstobeamixtureofAandB

26emsp|emspIsolation by distance and ecological divergence

Isolationbydistance(IBD)anddispersalbarriersareknowntocon-tribute toward the geographic structuring of genetic variation inmanyorganismsWethereforeusedtheIsolationByDistanceWebService323(JensenBohonaampKelley2005)toperformreducedmajoraxis regressionandMantel testsbasedon10000 randomi-zationsof thedatasetsGeographic great-circledistanceandpair-wise genetic distances between individuals were calculated usingtheGeographicDistanceMatrixGenerator123 (Ersts2016)andtheRpackageSTAMPP(Pembletonetal2013)respectivelyLocaladaptationcanalsobemanifestedincorrelationsbetweengeneticand environmental distances (FrankhamBallouampBriscoe 2002)WethereforeusedMantelandpartialManteltestsasimplementedintheRpackageVEGAN24-0(Oksanenetal2013)totestforcor-relationsbetweengenetic andenvironmental distances the latterbeinggeneratedusingtheldquodistrdquofunctioninRAsWashingtonia and Braheaareaffiliatedtohumidtropicalclimatesandarefrostsensi-tiveweexpectedclimaticvariablessuchasthemeantemperatureofthecoldestquarterprecipitationofthedriestquarterandthearid-ityindextohavethegreatestinfluenceonthesegeneraTheabove-mentionedecological informationwasthereforedownloadedfromWorldClimwiththeresolutionof30arc-seconds (~1km) (HijmansCameronParraJonesampJarvis2005)andfromtheGlobalAridityandPETdatabase(ZomerTrabuccoBossioampVerchot2008)asasetofrasterlayersManteltestswerethenperformedbetweeneachgeneticandenvironmentaldistancematrixandtheseanalyseswerealsorepeatedaspartialManteltestscontrollingforgeographicdis-tance Statistical significancewas determined using Pearson testsbasedon10000permutationsofthedata

27emsp|emspDetection of outlier loci associated with environmental variables

Environmental variables showing significant associations with ge-neticdistanceintheaboveanalyses(specificallymeantemperatureofthecoldestquarter inWashingtoniaandprecipitationinthedri-estquarterforBraheaseeSection3)werefurther investigatedbytestingforsignaturesof localadaptationusingtheRpackageLEA(Landscape Genomics and Ecological Association Test FrichotSchoville Bouchard amp Franccedilois 2013 Frichot amp Franccedilois 2015)andSAMβADA(Stuckietal2016)Thefirstoftheseprogramsuses


latentfactormixedmodelsLFMMstodetectlociexhibitingunusualassociationswithenvironmentalvariablescomparedtothegenomicbackgroundWe chose to use this program as it can account fortheunderlyingpopulationstructureby introducingldquolatentfactorsrdquowhilesimultaneouslyestimatingrandomeffectsduetopopulationhistoryand isolationbydistanceWe ran10000 iterationsof theGibbssamplingalgorithmwith the first5000 iterationsdiscardedasburn-inZscoresfromfiveindependentreplicaterunswerethencombinedandtheresultingp-valueswereadjustedforthefalsedis-covery rate (FDR) as described inBenjamini andHochberg (1995)withanalphalevelof005

ThesecondpackageSAMβADAimplementslogisticregressionstomodeltheprobabilityofobservingaparticulargenotypeateachmarkergiventheenvironmentalconditionsatthesamplinglocations(Joostetal2007)Wechosethemultivariateoptionasthisallowsacombinationofpredictorvariablestobesimultaneouslyassessedtherebyreducingtheoccurrenceofspuriousgenotypebyenviron-mentassociations (Stuckietal2016)ThetwopredictorvariablesforbothWashingtonia and BraheawerethegeneticgroupsidentifiedwithSPLITSTREEand the respectiveecological variable identifiedusingpartialMantel testsAnySNPsassociatedwiththemainge-neticgroupswere thendiscardedandonly thoseSNPsassociatedwithecologicalvariableswereretainedStatisticalsignificancewasdetermined using both log-likelihood ratio andWald tests (Joostetal2007)andFDRwasappliedtotheresultingp-valueswithanalphalevelof05

3emsp |emspRESULTS

31emsp|emspGenomic data

We subjected 190 palm samples to GBS generating a total of296358035 high-quality barcoded reads which were assembled

into 549976 tags that aligned uniquely to the P dactylifera refer-encegenomeFrom thesedatawecalleda totalof26565SNPsAfter quality filtering removing InDels retaining only bi-allelicnuclear SNPs LD filtering and removing lociwithmore than20missingdatathiswasreducedto2063SNPsdistributedover724scaffolds(median=oneSNPperscaffoldrange=1ndash30seeFigureS1)Thefinaldatasetcomprised514diagnosticSNPs(ie locithatwerefixedfordifferentallelesinthetwogenera)plus1549poly-morphicSNPsofwhich183werepolymorphicinbothgenera312werepolymorphiconlyinWashingtoniaand1054werepolymorphiconlyinBrahea(FigureS2)Additionallywegeneratedseparatedata-setsforeachpalmgenuscomprising85Washingtoniapalmsgeno-typedat1462polymorphicSNPsand79Braheapalms(excludingB edulis)genotypedat2050polymorphicSNPsObservedheterozy-gositywas lower inWashingtonia (0098 975CI=0089ndash0108)than in Brahea (0139 975 CI=0131ndash0146) while the oppo-site was found for expected heterozygosity (Washingtonia 0209975 CI=0200ndash0217 Brahea 0175 975 CI=0168ndash0182)Consistentwithdifferencesinobservedheterozygositythegenomicinbreeding coefficient Fhat3 was higher in Washingtonia (047 CI037ndash057)thaninBrahea(025CI021ndash029)

32emsp|emspPhylogenetic relationships

To elucidate taxonomic relationships we constructed a Bayesianphylogenetictreebasedonasubsetof54Washingtonia and Brahea individuals (Figure2) As expected the two genera were clearlyresolved as distinct and deeply divergent monophyletic clades(Figure2a)HoweverwheneachgenuswasanalyzedseparatelywefoundlittleevidenceinsupportofthemajorityofmorphologicallydefinedspeciesSpecificallyW filiferadidnotformamonophyleticgroupbutinsteadgroupedtogetherwithW robustapalmsfromthenorthernBajaCaliforniapeninsula(SSPSFSLandCAT)asshownin

F IGURE 2emspBayesianreconstructionofthephylogeneticrelationships(a)betweenWashingtonia and Brahea(b)withinWashingtonia(c)withinBraheaColoredlinesdelimitmorphologicallydefinedspeciesaccordingtoMinichetal(2011)andcoloreddotscorrespondtothesampledpopulationsMajornodeswithhighposteriorprobabilitysupport(gt095)areindicatedinasterisks()

(a) (b)

(c)


Figure2bFurthermoregreaterdivergencewasobservedbetweenW robustafromtheMexicanmainland(SON)anditspeninsularcon-specificsthanbetweenW filifera and W robustafromthenorthernBajaCaliforniapeninsulaThissuggeststhatanygeneticdifferencesbetweenW filifera and W robustaaresmallerthanthemagnitudeofintraspecificvariationwithinW robusta

BycontrasttwodistinctmonophyleticcladeswereresolvedinBrahea the first corresponding toB edulis fromGuadalupe IslandandthesecondcomprisingB armata and B brandegeei (Figure2c)Within the peninsular clade individuals diverged fromeach othernotbasedonmorphological speciesdesignationsbutaccording tothe sierras they were collected from On the bases of the aboveanalyseswethereforedefinedthreemajorpalmcladesontheBajaCaliforniapeninsulaandGuadalupeIslandcomprising(1)W robusta and W filifera(2)B brandegeei and B armataand(3)B edulis

33emsp|emspPopulation structure

NextwecarriedoutpopulationgeneticanalysestoinvestigatethecomparativepopulationstructureofWashingtonia and Braheapalmson the Baja California peninsula These analyses were conductedseparately for the two clades identified above corresponding toW robusta and W filifera(forthwithreferredtoasWashingtonia)andB brandegeei and B armata(forthwithreferredtoasBrahea)Strongpopulation structure was found in both genera with majority ofpairwisecomparisonsamongsierrasyieldingmoderately largeandhighlysignificantFstvalues(TablesS2andS3)ForWashingtoniathegreatestgeneticdifferenceswereobservedbetweenthepeninsularandmainlandlocalities(Fst=055ndash086p lt 001)aswellasbetweenthenorthernmostpopulationofSJandtheothersierras(Fst=046ndash086p lt 001)Additionallysierrasofthenorthern(CATSFSLandSSP) and southern (SGSM and SLL) regionsof theBajapeninsula

weresignificantlydifferentiatedfromoneanother(Fst=027ndash056p lt 01)whereasnegligiblestructurewasfoundwithineachoftheseregions (TableS2)Bycontrast inBrahea allpairwiseFst compari-sonsamongsierraswithinthepeninsulawerestatisticallysignificant(TableS3)

TouncoverthemaingeneticclusterspresentwithinWashingtonia and Brahea we used admixture estimation and individual cluster-ingwithinsNMFaswellasphylogeneticnetwork inferencewithinSPLITSTREE (see Section2 for details) Both of these approachesresolvedcleargroupingsandtherewasgeneralagreementbetweenthem on the strength and pattern of population structure In thecaseofWashingtoniafourmaindistinctgeneticclusterswererecov-ered (Figure3FigureS3) corresponding to (1) theMexicanmain-land(SON)(2)thesouthernBajapeninsula(SLLSM and SG)(3)thenorthernBajapeninsula (SSPSFSL and CAT)and (4)Washingtonia fromSierraJuarez(SJ)ForBraheathereweresomedifferencesintheresultsdependingontheanalyticalapproachusedSpecificallysNMF uncovered three distinct genetic clusters (Figure4a) repre-senting (1) the southernBaja peninsula (SLLSM and SSP) (2) thecentralBajapeninsula (SSFSLI and SA) and (3) thenorthernBajapeninsula (CATSSPM and SJ)BycontrasttheSPLITSTREEanaly-sis(Figure4b)wasmoresensitivetothephylogeneticstructuringofthepeninsularBraheapalmsandclearlypartitionedthesamplesintoninegeneticclusterseachcorrespondingtoadifferentsierraTheonlyexceptionsweretwosamplesfromSSFthatclusteredtogetherwithpalms fromSL two individuals thatweremisplacedbetweenSSF and SMandoneindividualbetweenSSP and SLIntriguinglyin-dividual clustermembership plots (Figure S3) also highlighted thepresenceofindividualpalmssampledfromthenorthernsierrasthatexhibitedcleargeneticancestryinthesouthernsierrasSpecificallyfourWashingtoniapalmssampledfromtwoofthenorthernsierras(CAT and SFSL)hadgenotypesindicativeofancestryinthesouthern

F IGURE 3emspPopulationstructureofWashingtoniapalmsPanel(a)showstheresultsofclusteranalysiswithinsNMFwithpiechartsindicatingthegeographicdistributionofsixinferredgeneticclusters(eachcodedbyadifferentcolor)Panel(b)showsaphylogeneticnetworkgeneratedbySPLITSTREE

(a) (b)


sierras SLL SM and SG whereas twoBrahea individuals sampledfromCAThadgeneticancestryconsistentwithSM and SLL


To investigate the potential cause of some individuals beingmis-assigned to their populations of origin we modeled populationdivergencewithmigrationwithinTREEMIXTheresultingmaximum-likelihood(ML)treeforWashingtoniawasconcordantwiththeprevi-ous results revealing deepdivergencebetween themainland andpeninsula populations and partitioning of the latter into southern(SLLSM and SG)andnorthern(SSPSFSLCAT)groups(Figure5a)Aftersequentiallytestingforbetweenoneandtendiscretemigra-tion eventswe found that the increase in likelihood beyond twomigrationeventswasclose to zero (FigureS4) and stepwisecom-parisonsoflog-likelihoodvalueslostsignificancebetweentwoandthree events (likelihood ratio testp gt 05) This indicates that themostlikelynumberofmigrationeventsamongthesierraswastwoExploringthisscenariofurtherwefoundevidenceforunidirectionallong-distancemigrationspanningaround450kmfromSGintoCAT and from SM into SFSL (Figure5a) These migration events werestronglysupportedbythree-populationtests(TableS4)

FortheBraheapalmsTREEMIXanalysissupportedthepartition-ingofthepeninsularsamplesintotwomajorgroupscomprisingthenorthernmost sierras (SJ and SSPM) and the rest of the peninsula(Figure5b)The latter inturnwaspartitionedintothenorthernsi-erras(SLSAandCAT)andthesouthernandmid-peninsulasierras(SLLSMSSPandSSF)InferredmigrationeventsforBraheapointedtowardthepossiblemigrationofpalmsbetweenthesouthernsierraofSMandthenorthernsierraofCAT(Figure5b)Howevertheover-allpatternofincreasingloglikelihoodwiththenumberofmigrationeventswas less pronounced than inWashingtonia (Figure S4) and

noneof themigrationeventsweresupportedbythree-populationtests(Zscoresltminus196)


Mantel tests revealed strong positive correlations between ge-neticandgeographicdistance forbothWashingtonia and Brahea (Mantelrsquos r=685p lt 0001 and r=609p lt 0001 respectivelyTable1) Furthermore Partial Mantel tests revealed significantassociations between genetic distance and environmental vari-ables after controlling for geographic distance Specifically themeantemperatureofthecoldestquartercorrelatedsignificantlywithgeneticdistanceinWashingtonia(PartialManteltestr=267p lt 0001)while the amount of precipitation in the driest quar-tercorrelatedsignificantlywithgeneticdistanceinBrahea(PartialManteltestr=09p=019)


In order to investigate the genomic basis of the associations de-scribedaboveweusedtwocomplimentaryapproachestotestforsignaturesoflocaladaptationinWashingtonia and BraheaFirstla-tentfactormixedmodelsLFMMswereusedtodetectlociexhibitingunusualassociationswithmeantemperatureofthecoldestquarterin Washingtonia and precipitation of the driest quarter inBrahea This resulted in the identificationof80SNPs inWashingtonia and 51SNPsinBraheaaftertable-widecorrectionofthecorrespondingp-valuesforthefalsediscoveryrateSecondweusedamultivariateapproachimplementedinSAMβADAtotestforgenotypebyenvi-ronmentassociationsThisapproachidentified18significantasso-ciationsinWashingtonia and none in Brahea

F IGURE 4emspPopulationstructureofBraheapalmsPanel(a)showstheresultsofclusteranalysiswithinsNMFwithpiechartsindicatingthegeographicdistributionofthreeinferredgeneticclusters(eachcodedbyadifferentcolor)Panel(b)showsaphylogeneticnetworkgeneratedbySPLITSTREE

(a) (b)


FinallyweaskedwhethertheoutlierlociidentifiedbyLFMMandSAMβADA (totaln=97 forWashingtonia and51 forBrahea) resolvecontrastingphylogeniestotheneutralloci(definedasthoselocithatwerenotidentifiedbyeitherprogramn=1365forWashingtonia and 1999forBrahea)AnalysiswithinSPLITSTREErevealedastrikingpat-tern forWashingtonia inwhich theneutral loci resolvedfourgroupscorrespondingtothesouthernBajapeninsula (SLLSMandSG) thenorthernBajapeninsula(SSPSFSLandCAT)SJ and SON(Figure6a)

whereastheoutlier locionlyresolvedtwogroupscorrespondingtothe southern Baja peninsula combinedwith SON and the northernBajapeninsulacombinedwithSJ(Figure6b)Phylogenetictreescon-structedfromthesamenumberofrandomlyselectedneutral lociasthereareoutliersalsorecoveredfourpopulations(FigureS5)suggest-ingthatthecontrastingtopologiesrecoveredbytheoutlierandneu-trallociareunlikelytobecausedbydifferencesinresolvingpowerBycomparisonthemaindifferencebetweentheneutralandoutliertreesforBraheawasthattheformerresolvedindividualsierras(FigureS6a)whereasthelatterdidnot(FigureS6b)Thisappearstoberelatedtogeneticresolutionasphylogenetictreesbasedonthesamenumberofrandomlyselectedneutrallociasoutliersalsofailedtoclearlyresolvethesierras(FigureS7)

4emsp |emspDISCUSSION

Comparative studies can provide valuable insights into processesthatshapepopulationgeneticstructureandtherebyhelptoimproveour understanding of how organisms may respond to ongoingenvironmental change We therefore used GBS both to resolvetaxonomic uncertainties and to characterize patterns of population

F IGURE 5emspMaximum-likelihoodtreesdepictingpatternsofgeneticdivergenceamong(a)Washingtoniapalmsgroupedintoeightpopulationsand(b)Braheapalmsgroupedintotenpopulations(seeSection2fordetails)Inferredmigrationeventsareindicatedbydashedlineswiththedirectionofgeneflowindicatedbyarrowsandcolorintensityreflectingtheintensityofgeneflow

(a)

(b)

Washingtonia Brahea

Mantel Partial Mantel Mantel Partial Mantel

Geographicdistance 0685 NA 0609 NA

Aridity minus0059 minus0180 0068 minus0230

Meantemperatureofthecoldestquarter

0620 0267 0248 minus0160

Precipitationofthedriestquarter

0177 0010 0127 009

TABLE 1emspMantelandpartialManteltestssummarizingrelationships(r and associatedpvalues)betweengeneticdistancegeographicdistanceandclimatevariablesinWashingtonia and Brahea P-values P lt 005 P lt 001 P lt 0001

F IGURE 6emspPhylogeneticnetworksconstructedseparatelyforWashingtoniausing(a)neutralloci(b)outlierloci


structure in two closely related North American palm generaWashingtonia and Brahea on theBajaCalifornia peninsula adjacentMexican mainland and Guadalupe Island Bayesian phylogeneticanalysis supported the classification of B edulis as a distinctspecies but this was not the case for W filiferandashW robusta and B armatandashB brandegeei Furthermore population genetic analysesclustered the peninsularWashingtonia palms into two populationscorresponding to the northern and southern peninsula whereasin Brahea every sierra could be genetically distinguished We alsodetected a relatively strong influence of ecologically mediateddivergence in Washingtonia palms with outlier loci correlated totemperatureresolvingamarkedlydifferentphylogenetictreetoneutrallociFinallywe foundevidence for twounidirectional long-distancemigrationeventsinWashingtoniainlinewiththeprevioussuggestionthat human-mediated dispersal could have been disproportionatelyimportantinthisgenus(McClenaghanampBeauchamp1986Minnichetal 2011) None of these patterns could previously be detectedusingeitherallozymes(McClenaghanampBeauchamp1986)orclassicalplastid and nuclear markers (Klimova etal 2017) suggesting thatGBSandrelatedapproachesrepresentpowerfultoolsforuncoveringecologicallyrelevantpopulationsubdivision


Thefirstaimofourstudywastoresolvephylogeneticrelationshipsbetween andwithinWashingtonia and Brahea palms sampled fromthe Baja California peninsula and adjacent areas As expected thetwogenerawerefoundtobedeeplydivergentconsistentwiththeirhavingseparatedfromoneanotheratleast25ndash35millionyearsago(Baconetal2012BakerampCouvreur2013Howevermixedsupportwas found for currently recognized taxonomic relationships withineach genus (Felgeramp Joyal 1999Henderson etal 1995Minnichetal 2011) Starting with Washingtonia Bayesian phylogeneticreconstructionuncoveredtwomainlineagesthefirstcorrespondingtoW robusta from the north of the Baja peninsula together withW filifera and the second corresponding to W robusta from thesouthern Baja peninsula and the Mexican mainland FurthermorethemagnitudeofdivergencebetweenW filifera and W robustafromthe northern Baja peninsula was lower than that found betweenW robusta from the northern Baja peninsula and the Mexicanmainland(ieitwaswithintherangefoundwithinasinglespecies)Ourdatatherefore leadustotheconclusionthatW filifera ismorelikelytorepresentthenorthernmostpopulationofW robustathanaseparatespeciesThisisinlinewithapreviousstudybyBaconetal(2012)whofoundnodifferencesbetweenW filifera and W robusta atthreeplastidandthreenucleargenesandisalsoconsistentwithanapparent lackof reproductive isolationbetweenthesepalmsashybridization is common in cultivation (Hodel 2014) Furthermorea highly detailed morphological study ofWashingtonia palms from17 sites on the peninsula recently found no clear support for twodistinct species based on 11 morphological characteristics butrather suggested the presence of a latitudinal morphological cline(Villanueva-AlmanzaampEzcurra2017)

Bayesian phylogenetic reconstruction of Brahea provided evi-denceinsupportofthespeciesstatusofGuadalupeIslandpalms(B edulis)althoughthiswastosomeextentexpectedgiventhegeolog-icaloriginandgeographicisolationofGuadalupeIsland(AleixandreHernandez-Montoya amp Mila 2013 Karhu Vogl Moran Bell ampSavolainen2006Klimovaetal2017)Nonethelessourdatadidnot support the recognition of two separate speciesB armata in thenorthernpeninsulaandB brandegeeiinthesouthernpeninsulaAgainthisisconsistentwithapreviousgeneticstudybasedonchlo-roplastandnuclearsequenceswhichalsofailedtoseparatethepen-insularBraheaintotwomonophyleticgroups(Klimovaetal2017)Onereasonforthiscouldbethattheoriginaltaxonomywasbasedonrelativelysubtlemorphologicaldifferencessuchasleafcolorationand inflorescence architecture (Felger amp Joyal 1999 Hendersonetal1995)andthesetraitscouldpotentiallyshowplasticvariationamongpopulationsinresponsetotheprevailingenvironmentalcon-ditions(RoncalHendersonBorchseniusCardosoampBalslev2012)Oneway to test thishypothesiswouldbe touse reciprocal trans-plantorcommongardenexperiments

42emsp|emspPatterns of population genetic structure

Washingtonia and Brahea palms from theBajaCaliforniapeninsulaprovideauniqueopportunitytoexplorethecontributionsofmulti-plepotentialdriversofpopulationstructurewithinanunusuallyhet-erogenousnaturalsettingHoweverarecentstudybasedonnuclearandchloroplastgeneswasunabletorecoversufficientlevelsofpol-ymorphismtoprovideinsightsatthepopulationlevel(Klimovaetal2017)FortunatelyGBSallowedustogenotypeover25000SNPswhichafterhighlystringentfilteringtoretainonlypolymorphicun-linkedlociwithasmallproportionofmissingdataleftuswithatotalof1462and2050genome-widedistributedSNPsinWashingtonia and BrahearespectivelyThesedataallowedustouncovercontrast-ingandinsomecasesunexpectedpatternsofgenomewidedifferen-tiationwithWashingtoniapopulationsshowingaclearnorthndashsouthsplitwhereasinBraheaeachindividualsierracouldberesolved

WefoundevidenceforfourmaingroupsofWashingtoniapalmsAs might be expected given the degree of geographic isolationpalmsfromtheMexicanmainlandandSJformedseparateclustersbutwedidnotanticipatefindingtwodistinctpalmlineagesamongsierras of the Baja California peninsula that were roughly evenlyspacedalonga latitudinalclineManyplantandanimal speciesonthepeninsulashowasimilarnorthndashsouthdividethathasbeenlinkedtothetemporaryformationofamid-peninsulaseawayaroundamil-lionyearsago(Lindelletal2006Riddleetal2000)Howeverthisisnotstrictlyconsistentwithour resultsaspalms fromSSP show membershiptothenorthernclusterbutarelocatedtothesouthofwheretheseawayisbelievedtohavebeenlocatedThereasonsforthisarenotentirelyclear It ispossiblebut fairlyunlikely that thetruelocationoftheseawaywasactuallyfurthersouththaniscur-rentlybelievedAlternativelyWashingtoniacouldhavebeenlocallyextirpatedatSSPandsubsequentlyrecolonizedfromSFSLaftertheclosure of the seaway This explanation is plausible both because


ecologicalnichemodelinghasshownmajorshiftsinthedistributionofsuitablehabitatoverthepast100000yearsandSSPiscurrentlyrepresentedbyasingle isolatedoasissituatedonthemarginsofalargeareaofunsuitablehabitat(seeFigure6inKlimovaetal2017)

Our results for Brahea are in many respects more readily ex-plained (Klimova etal 2017) SPLITSTREE partitioned the palmsintoninegeneticclusterseachcorrespondingtoadifferentsierrawhile sNMF detected three main groups whose frequencies fol-lowedaclearclinealongthepeninsulaconsistentwithasignificantpattern of isolation by distance (Mantelrsquos r=609 p lt 001) ThisprobablyreflectsthefactthattheseedsofBraheapalmsareprimar-ilydispersedbywaterpulsesthatwashthemshortdistancesalongcanyons(WehnckeampLoacutepez-Medelliacuten2014Wehnckeetal2009)BycontrastWashingtoniapalmshaveediblefruitthatareeatenbybirdsandsmallmammalsandwhichwereapparentlyalsousedbyindigenouspeople(Cornett2008Luna2012)therebyfacilitatingthedispersalofintactseedsbetweenadjacentoases

AnotherfactorthatcouldhavecontributedtowarddifferencesbetweenWashingtonia and Brahea is demographic history In par-ticular historical bottlenecks can lead to strong genetic drift andtherebycontributetowardboththepatternandstrengthofpopula-tiongeneticstructure(FutuymaampKirkpatrick2017)Unfortunatelyhowever GBS and related approaches are not well suited to de-mographic reconstruction as tests for bottlenecks and populationexpansion are extremely sensitive to MAF thresholds and otheraspects of the bioinformatic pipeline(s) used (Shafer etal 2017)Neverthelesswehavelittlereasontobelievethatthetwogeneraexperienced markedly different recent demographic histories asecological nichemodeling has shown that bothWashingtonia and Brahea would have been locally restricted to similar areas duringtheLGM(about22000yearsago)andsubsequentlyre-establishedthemselvesacrossmostofthepeninsula(Klimovaetal2017)

43emsp|emspEcologically mediated divergence

Thereisgrowinginterestandempiricalsupportforthenotionthatstrong divergent natural selection can drive genomic divergenceultimatelyleadinginsomecasestoreproductiveisolationandspe-ciation (BeheregarayCookeChaoampLandguth2015Lexeretal2014Sorketal2016)ThepalmsofBajaCaliforniaareinterestingin this regardbecause they reside at theextremenortherndistri-butional limitsof themostly tropicalArecaceaeandare thereforesubjected to unusually dry cold and generally suboptimal condi-tions(HampeampJump2011WoolbrightWhithamGehringAllanampBeiley 2014)Under such conditions local adaptation can be aparticularlyimportantforceinshapingpatternsofdivergenceacrossthegenome(PannellampFields2014SavolainenLascouxampMerilauml2013)Ourresultsareconsistentwiththisnotionandsuggestthatlocaladaptationmayhavecontributedtowardthepopulationstruc-tureofWashingtoniainparticular

We originally hypothesized that the influence of ecologicallymediatedselectionshouldbestrongestonWashingtoniapalmsdueto their stricter ecological requirements and relatively restricted

geographicdistribution (Minnichetal 2011) In linewith thiswedetectedsignificantassociationsbetweenenvironmentalvariablesand genetic distance in both genera but these were stronger inWashingtoniaWealso found that geneticdistancewas correlatedto the mean temperature of the coldest quarter inWashingtoniawhereas in Braheageneticdistancewasassociatedwithprecipita-tionofthedriestquarterTakenatfacevaluethisdifferencewouldimplythateventhoughmanyoftheWashingtonia and Braheapalmsweresampledfromthesameoasesnaturalselectionhasinfluencedthetwogeneraindifferentways

Toexplorethisfurtherweusedtwodifferentapproachestotestforlocishowingunusualassociationswithenvironmentalvariables Inbothcasesweattemptedtominimizetheoccurrenceoffalsepos-itiveseitherbycontrollingfortheunderlyingpopulationstructureby introducing latent factors (inLEA)orusingmultivariate logisticregression(inSAMβADA)whichreducestheoccurrenceofspuriousgenotype by environment associations (Stucki etal 2016) Theseapproaches identified different sized and largely non-overlappingsubsetsof locibutthis isconsistentwithpreviousstudiesandre-flectsdifferencesintheunderlyingmethodologiesandassumptions(Benestanetal2016FengJiangampFan2016NadeauMeirmansAitkenRitlandampIsabel2016)Tocaptureasmanyoutliersaspos-siblewethereforepooledallofthelociflaggedbyatleastoneap-proach and classified the remaining loci as neutral ConstructingphylogenetictreesseparatelyforthesetwoclassesoflocusrevealedacleardifferenceinWashingtoniawiththeneutrallociresolvingfourgroupsbuttheoutlierlocionlytwogroupsThisfindingisreminis-centofsimilarstudiesthatlikewiseresolveddifferenttreesbasedonneutralandoutlierloci(Funketal2016Kelleretal2013MatalaAckermanCampbelampNarum2014)Suchapatterncouldbecon-sidered a footprint of selection asSJ and thenorthernpeninsularsierrashavedivergedatthegenomicbackgroundwhilestabilizingselectionappearstohaveresultedinverysimilargenotypesattheoutlierloci

The equivalent results for Brahea were less clear cut WithintheBaja peninsula the outlier loci failed to resolve the individualsierrasHoweverphylogenetictreesbasedonthesamenumberofrandomly selected neutral loci also grouped the sierras togethersuggestingthatgeneticdifferencesbetweenthesierrasmaybetooweaktoberesolvedbyarelativelysmallsubsetofSNPsEitherthiscouldreflectweakerselectivepressuresonBraheapalmsoralterna-tivelytheassociationbetweengeneticdistanceandprecipitationofthedriestquarterinBraheacouldbeatypeIerrorFurtherinsightsintothisandrelatedquestionscouldbegainedfromdetailedphys-iologicalstudiesaimingtoestablishmoreclearlyhowthetwopalmgenerarespondtoclimaticextremes

44emsp|emspPatterns of long- distance dispersal

A furtherunexpectedpatternwas revealedbycluster analysesoftheGBSdataOverallthemajorityofindividualswereconfidentlyclustered to their respective geographic groups and levels ofadmixturebetweenthe identifiedpopulationswere lowHowever


several palms sampled from the northern sierras had genotypesthatwereclearlyconsistentwithancestryinthesouthernsierrasapatternthatisstronglysuggestiveofrecentlong-distancedispersalToexplore this furtherweusedTREEMIX to infer themost likelynumber ofmigration events in both palm species The results forWashingtoniawere clear cutwith strong support being found fortwo distinct south to north migration events spanning around450kmBycontrastalthoughonemigrationeventwasinferredforBraheathiswasnotsupportedbythree-populationtestsandshouldthereforebetreatedasputativeatbest

It is unlikely that these patterns could have resulted fromdifferences in the natural dispersal abilities of the two palmgenera because even though Brahea is more dispersal limitedWashingtoniacannotbenaturallydispersedovermorethanafewtens of kilometers Furthermore if natural agents such as birdsormammalswere involvedonewouldnotnecessarilyexpect tofindabiasinthedirectionofmigrationfromnorthtosouthwhichappears to be the case for the long-distance migration eventsinferred inWashingtoniaHowever as palmshave a longhistoryofrelationshipwithhumansandhavebeenextensivelyusedasasource of food constructionmaterials andmore recently as or-naments in cities and gardens several authors have speculatedthat humansmayhavebeen involved in spreadingpalmson theBajapeninsula (Cornett2008FelgerampJoyal1999Levisetal2017 McClenaghan amp Beauchamp 1986 Minnich etal 2011)FurthermorethefruitsofWashingtoniawereextensivelyusedasafoodsourcebynativepeople(Cornett1987FelgerampMoser1985FelgerampJoyal1999)whereasBraheafruitwerelessappreciatedandhaveevenbeenreferredtoasldquouselessrdquo(Minnichetal2011)leadingsomeauthorstosuggestthattheindigenouspeopleoftheBaja peninsulamayhavedispersedWashingtonia but notBrahea prior to European contact (Cornett 2008Minnich etal 2011)Ourresultsareconsistentwiththishypothesisaslong-distancemi-grationeventswereonly inferredunequivocally inWashingtonia HoweverthetwonorthernoasescontainingWashingtoniapalmsofsouthernancestryarealsobothsitesofcolonialSpanishmis-sionswhereagricultureandtradewouldhavebeenespeciallywelldeveloped(Minnichetal2011)Consequentlyitisnotinconceiv-able that these genetic introductions could have occurredmorerecentlywhichissupportedbytheobservationthatthepalmsinquestionexhibitednegligibleadmixtureAlthoughthereareclearprecedents for human-mediated dispersal of palms (Aschmann1957 Kondo etal 2012 Rivera etal 2013) we prefer not tospeculate further at this point without additional archeologicalevidenceormoredetailedgeneticdatathatwouldallowustoreli-ablydatethesemigrationevents

45emsp|emspLimitations of the study

The recent development of cost-effective methods for obtaininghigh-quality genome-scaledatahas stimulatedgrowing interest inthe genomic basis of ecological divergence By greatly increasinggenotypingcoverageapproacheslikeGBShavemadeitpossibleto

identifygenomicregionsandinsomecasesspecificlociresponsibleforadaptivedifferencesamongpopulations(Savolainenetal2013)NonethelessanumberofcaveatsneedtobetakenintoaccountForexamplepopulationstructuredemographichistoryandthequalityoftheenvironmentaldataandbiasescausedbythegeneticmark-ersthemselvescanallleadtofalse-positiveresultsinoutlierscans(Hobanetal2016)

First of all disentangling IBE from neutral patterns of geneticvariationcanbechallenging(WangampBradburd2014)becauseIBDcanproducepatterns similar to IBEwhengeography is correlatedwithenvironmentalvariation(Meirmans2012Nadeauetal2016)Weattemptedtoreducethispotentialsourceofbiasbyanalyzingonlyecologicalvariablesthatweresignificantlyassociatedwithge-neticdistanceafterhavingcontrolledforgeographicdistanceWefurtherminimizedtheoccurrenceoffalsepositivesbycontrollingforpopulationstructureanddemographichistorybyintroducinglatentfactorsintotheLEAanalysisandbyimplementingamultivariatelo-gisticregressionapproachinSAMβADA

Second theaccuratedetectionof locallyadapted loci throughgenotypendashenvironment associations also depends on accuratemeasures of different aspects of the ecological landscape Low-resolutionenvironmentaldatamay reduce theaccuracyof resultseveniftheselectiveenvironmentisknown(Hobanetal2016)sothe resolution of the environmental datamust be fine enough toadequatelycharacterizeeachsamplinglocalityForthisreasonwecross-referenced fine resolution (~1km scale) environmental datawithGPScoordinatescollectedbyourselvesateachoasis

Third in commonwith virtually all genotyping approaches in-cluding restriction enzyme-based methods GBS suffers from anumber of potential sources of genotyping error (Andrews etal2016Hobanetal2016)OneofthemostimportantoftheseisthepresenceofnullallelesTheseoccurwhenapolymorphismwithintherestrictionenzymerecognitionsiteresults infailuretocutthegenomicDNAatthat locationAlleles lackingthecompleterecog-nitionsitearenotsequencedwhichresults in individualswhoareheterozygousforthenullalleleappearingashomozygotesNullal-lelescandownwardlybiasestimatesofgeneticdiversityoveresti-mateFstandresultinanincreaseinfalsepositivesinFstoutliertests(Andrews etal 2016) To overcome this limitation we used twoapproachesthatdetectassociationsbetweengeneticandenviron-mentaldistanceswithoutestimatingFst (FrichotampFranccedilois2015Stuckietal2016)

ArelatedissueisthatstochasticprocessesduringPCRcancauseoneallele toamplifymore readily than theotheratagiven locusThis can lead to downstreamgenotyping errors as heterozygotescanappearashomozygotesorallelescontainingPCRerrorscanbeinterpretedastrueallelesHoweveratleastintheoryPCRshouldnotsystematicallyfavoronealleleoveranotheratagivenlocusandthereforeparametersestimatedfromalargenumberoflociareun-likelytobesubstantiallybiased(Andrewsetal2016)FurthermorealthoughreducedgenomerepresentationapproachessuchasGBSprovidefargreatergenomiccoveragethantheirpredecessorssuchas microsatellites or amplified fragment length polymorphisms


it isnevertheless importanttobear inmindthatonlyafractionofthegenomecanbescreenedwhichmayresult insomeimportanttargets of selection being missed (Narum Buerkle Davey MillerampHohenlohe2013)Howeverweweremore interested inbroadpatternsrather than in thenatureof thespecific lociunderselec-tion and the contrasting topographies of neutral versus selectedloci in Washingtonia suggest that at least for this genusour studywassuccessfulatdetectinggenomicregionsinfluencedbyselectionClassical approaches like common garden or reciprocal transplantexperimentswouldprovideasuitablebasisforfutureconfirmatorystudies(Andersonetal2010Savolainenetal2013)

5emsp |emspCONCLUSIONS

Comparative studies can shed light on species-specific propertiesthat may influence dispersal and ecological divergence while GBSoffersanunprecedentedlydetailedwindowongenome-widepatternsof differentiation By combining these approaches in iconic NorthAmericanpalmswewereabletouncovermarkedlydifferentpatternsofpopulationstructureinWashingtonia and Brahearevealassociationsbetweengenetic distance and climaticvariables identify subsets oflocithatappeartobeunderdivergentecologicallymediatedselectionand identify long-distancemigrationevents consistentwithhuman-mediateddispersalNoneof these patterns could be detectedwithclassicalmolecularmarkersindicatingthepromiseofapproacheslikeGBStodissectapartthecontributionsofdifferentprocessestowardgenome-widepatternsofdivergence

ACKNOWLEDG MENTS

The authors are grateful to Alfonso Medel Narvaacuteez RaymundoDomiacutenguez Cadena and Julio Montoya for participating in thecollection of samples We also thank Dr Jesus Neftali GutierrezRivera from Centro de Investigaciones Biological del Noroeste forcontributing toward the laboratory part of the research LogisticsupportforcollectingonGuadalupeIslandandSierraLaLibertadwasprovidedbytheGrupodeEcologiacuteayConservacioacutendeIslasandVictorSanchez Sotomayor respectivelyThisworkwas funded by projectsRedTemaacuteticadeInvestigacioacutenCONACyT280030andtheCONACyTBasicScienceproject251919WearealsothankfultoDrsEduardoVivas Pedro Pentildea Garcillaacuten Christine Bacon and two anonymousrefereesforprovidinghelpfulcommentsonthemanuscript

CONFLIC T OF INTERE S T

None declared

AUTHOR CONTRIBUTIONS

AK AOR and JIH designed the research AK collected samplesAK performed molecular laboratory work AK DLJV and JIHanalyzed the molecular data AK and JIH wrote the manuscript

AORprovidedfundingallauthorsapprovedofthefinalversionofthemanuscript

DATA ACCE SSIBILIT Y

Allofthegenotypestogetherwithenvironmentaldataforthesam-pling locations are available from Dryad httpsdoiorg105061dryad5vk6219

ORCID

Anastasia Klimova httporcidorg0000-0002-1502-2910

Alfredo Ortega-Rubio httporcidorg0000-0002-6365-287X

Joseph I Hoffman httporcidorg0000-0001-5895-8949

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RiddleBRHafnerDJAlexanderLFampJaegerJR(2000)Crypticvicariance inthehistoricalassemblyofaBajaCaliforniapeninsulardesertbiotaProceedings of the National Academy of Sciences of the United States of America9714438ndash14443httpsdoiorg101073pnas250413397

RiemannHampEzcurraE(2007)Endemicregionsofthevascularfloraof the peninsula of Baja California Mexico Journal of Vegetation Science 18 327ndash336 httpsdoiorg101111j1654-11032007tb02544x

RiveraDJohnsonDDelgadilloJCarrilloMHOboacutenCKruegerR hellipCarrentildeo E (2013)Historical evidence of the Spanish intro-duction of date palm (Phoenix dactylifera L Arecaceae) into theAmericas Genetic Resources and Crop Evolution 60 1433ndash1452httpsdoiorg101007s10722-012-9932-5

RokasAampCarrollSB (2005)Moregenesormore taxaThe rela-tivecontributionofgenenumberandtaxonnumbertophylogeneticaccuracyMolecular Biology amp Evolution221337ndash1344httpsdoiorg101093molbevmsi121

RoncalJHendersonABorchseniusFCardosoSRSampBalslevH(2012)Canphylogeneticsignalcharacterdisplacementorrandomphenotypic drift explain the morphological variation in the genusGeonoma (Arecaceae)Biological Journal of the Linnean Society106528ndash539httpsdoiorg101111j1095-8312201201879x

RundleHampNosil P (2005) Ecological speciationEcology Letters8336ndash352httpsdoiorg101111j1461-0248200400715x

Savolainen V Anstett M C Lexer C Hutton I Clarkson J JNorupMVampBakerW J (2006)Sympatric speciation inpalmson an oceanic island Nature441210ndash213httpsdoiorg101038nature04566

SavolainenOLascouxMampMerilaumlJ(2013)EcologicalgenomicsoflocaladaptationNature Reviews Genetics14807ndash820httpsdoiorg101038nrg3522

SchluterD(2000)The ecology of adaptive radiationOxfordUKOxfordUniversityPress

Shafer A B A Peart C Tusso SMaayan I Brelsford AWheatC ampWolf J BW (2017) Bioinformatic processing of RAD-seqdata dramatically impacts downstream population genetic in-ference Methods in Ecology amp Evolution 8 907ndash917 httpsdoiorg1011112041-210X12700

ShaferABAampWolfJBW(2013)Widespreadevidenceforincip-ient ecological speciationAmeta-analysis of isolation-by-ecologyEcology Letters16940ndash950httpsdoiorg101111ele12120


Silverstein R P (2005)Germination of native and exotic plant seedsdispersed by coyotes (Canis latrans) in Southern California The Southwestern Naturalist50472ndash478httpsdoiorg1018940038-4909(2005)050[0472GONAEP]20CO2

SorkVLGuggerPFChenJMampWerthS (2016)Evolutionarylessons from California plant phylogeography Proceedings of the National Academy of Sciences of the United States of America 1138064ndash8071httpsdoiorg101073pnas1602675113

SpinksPQThomsonRCampShafferHB (2014)Theadvantagesof going large Genome-wide SNPs clarify the complex popula-tion history and systematics of the threatenedwestern pond tur-tle Molecular Ecology 23 2228ndash2241 httpsdoiorg101111mec12736

StuckiSOrozco-WengelPForesterBRDuruzSColliLMasembeChellipJoostS(2016)Highperformancecomputationoflandscapege-nomicmodelsincludinglocalindicesofspatialassociationMolecular Ecology Resourceshttpsdoiorg1011111755-099812629

Tomlinson P B (2006) The uniqueness of palms Botanical Journal of the Linnean Society 151 5ndash14 httpsdoiorg101111j1095-8339200600520x

Tregear J W Rival A amp Pintaud J C (2011) A family portraitUnravellingthecomplexitiesofpalmsAnnals of Botany1081387ndash1389httpsdoiorg101093aobmcr269

VendramiD L J Telesca L SchweyenHWeigandHWeissMFawcettKhellipHoffmanJI(2017)RADsequencingresolvesfine-scalepopulationstructureinabenthicinvertebrateImplicationsforunderstandingphenotypic plasticityRoyal Society Open Science4160548httpsdoiorg101098rsos160548

Villanueva-AlmanzaLampEzcurraE(2017)Historia botaacutenica temprana y variacioacuten clinal del genero Washingtonia (Arecaceae)XIVSimposiodeBinacionaldeBotaacutenicaBajaCaliforniayAacutereasAdyacentes

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WehnckeEVampLoacutepez-MedelliacutenX(2014)LivingattheedgeBluefanpalmdesertoasesofnorthernBajaCaliforniaInEVWehnckeSAlvarezBorregoampEEzcurra(Eds)Conservation science in Mexicorsquos Northwest ecosystem status and trends in the Gulf of California (pp217ndash234)MexicoMexicoInstitutoNacionaldeEcologigraveayCambioClimagravetico

WehnckeEVLoacutepez-MedelliacutenXampEzcurraE(2009)Patternsoffru-givoryseeddispersalandpredationofbluefanpalms(Brahea armata)inoasesofNorthernBajaCaliforniaJournal of Arid Environments73773ndash783httpsdoiorg101016jjaridenv200903007

WehnckeEVLoacutepez-MedelliacutenXampEzcurraE(2010)Bluefanpalmdistribution and seed removal patterns in three desert oases ofnorthernBajaCaliforniaMexicoPlant Ecology2081ndash20httpsdoiorg101007s11258-009-9682-4

Wiggins I L (1980) Flora of Baja California Stanford CA StanfordUniversityPress

Wollstein A amp Lao O (2015) Detecting individual ancestry in thehumangenomeInvestigative Genetics61ndash12

WoolbrightSAWhithamTGGehringCAAllanGJampBeileyJK(2014)ClimaterelictsandtheirassociatedcommunitiesasnaturalecologyandevolutionlaboratoriesTrends in Ecology amp Evolution29406ndash416httpsdoiorg101016jtree201405003

WrightS(1943)IsolationbydistanceGenetics28114ndash138ZomerRJTrabuccoABossioDAampVerchotLV(2008)Climate

change mitigation A spatial analysis of global land suitability forclean development mechanism afforestation and reforestationAgriculture Ecosystems amp Environment 126 67ndash80 httpsdoiorg101016jagee200801014

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleKlimovaAOrtega-RubioAVendramiDLJHoffmanJIGenotypingbysequencingrevealscontrastingpatternsofpopulationstructureecologicallymediateddivergenceandlong-distancedispersalinNorthAmericanpalmsEcol Evol 2018001ndash18 httpsdoiorg101002ece34125


1emsp |emspINTRODUC TION

Comparativephylogeographic studiesof codistributed species areof paramount importance in decoding how shared geological andecological histories may have affected contemporary species andpopulations (Papadopoulou amp Knowles 2016) By comparing thespatial genetic structure of multiple codistributed species com-parative studies allow the assessment of phylogeographical con-gruencewhich is a baseline for historical inference (Avise 2000GarrickRowellSimmonsHillisampSunnucks2008Hickersonetal2010HoffmanClarke LinseampPeck2011)Moreover a generalunderstanding of how species and populations responded to pastchallengesmightprovideuswithinsightsintohowpresentandfu-turehumanactivitieswillimpacttheplanetsbiota(AviseBowenampAyala2016)

Itisalsobecomingincreasinglyrecognizedthatinteractionsbe-tweenorganismsandtheirenvironmentcanshapethedistributionofspatialgeneticvariationandleadtolocaladaptation(AndersonWillisampMitchell-Olds2011)Thisinturnmayreducetheamountofgeneflowbetweenpopulationsultimatelyputtingthemonthepathto speciation (RundleampNosil 2005 Schluter 2000) Theprimarydifference between ecologically mediated divergence and neutraldivergenceisthattheformerresultsinapatternofisolationbyen-vironment (IBE) inwhichgenetic andenvironmental distances arepositivelycorrelatedindependentlyofgeographicdistance(ShaferampWolf2013WangampBradburd2014)Bycontrasttheneutraldiver-gencemodelemphasizestheroleofgeographicisolationinrestrict-ingtheexchangeofmigrantsbetweenpopulationswhichresultsinapatternofisolationbydistance(IBD)thatisfrequentlyobservedinnaturalpopulations(Prunieretal2017Wright1943)

Althoughspeciesthatsharethesamelandscapemayfacesimilarselective environments their capacity to adapt to these environ-mentsmaybespecies-orevenpopulation-specificandcandependon both extrinsic and intrinsic factors including the strength andnature of selection the amount of genetic diversity and the ex-tentofphenotypicplasticity (SorkGuggerChenampWerth2016)Consequentlyspeciesinhabitingacommonlandscapemayvaryintheircapacitytoadapttoecologicalgradientsandchangingenviron-mentsAssessingadaptiveresponsesamongrelatedspecieswithinsharedheterogeneous landscapesmaythushelpustounderstandpatternsofbiodiversityAmajorsteptowardthisgoalisidentifyingtowhat extent ecology gene flow and genomic architecture con-tributetowardvariability intheevolutionarypotentialofmultiple-relatedspecies inhabitingthesame landscape (Raeymaekersetal2017)

In this regard theBajaCaliforniapeninsulawith itsheteroge-neousarrayoflandscapesandhabitatsvaryingfromtropicaldecid-uousforestsandmesicoasestoxericdesertscrubmountainsandlowaltitudearidplainsisofparticularinterest(DolbyBennettLira-NoriegaWilderampMunguia-Vega2015)Thepeninsulawasformedaround5ndash10millionyearsago(mya)whentectonicforcesgaverisetotheGulfofCaliforniaandseparatedanarrowsectionoflandfromtheMexicanmainlandCurrentlyaseriesofmountainrangesmost

prominentlySierraSanPedroMartirSierraLibertadandSierraLaGigantaruninsuccessionalongthepeninsulafromnorthtosouthIthasbeensuggestedthattheupliftofthesemajorsierrasprobablybeganaround6ndash10myaandthattheirformationwastieddirectlytothesametectonicforcesthatopenedtheGulfofCaliforniaandcre-atedtheSanAndreasFaultsystem(Martiacuten-Barajas2014MuellerKier Rockwell amp Jones 2009) Together the sierras constitute amoreorlesscontinuousmountainousbackbonethatseparateseco-systemsslopingeastintotheGulfofCaliforniafromthoserunningwestwards into the Pacific and also creates a complex landscapegradientalongtheentirepeninsularthatisreflectedinaveryhighdiversityofenvironments (RiemannampEzcurra2007)Thisuniquenatural setup characterizedbyunusuallyhigh levelsofboth land-scapeandecologicalcomplexitycouldconceivablyshapethepopu-lationstructureofspeciesinhabitingthepeninsulaviabothneutralandecologicallymediatedprocesseswiththeirrelativeimportancedepending on intrinsic qualities of the species in question (Dolbyetal2015)

AnadditionaldimensionisprovidedbythemorerecenthistoryoftheBajaCaliforniapeninsulawhichexperiencedanotableeco-logicalshiftinvolvingprogressivearidificationaftertheLastGlacialMaximum(LindellNgoampMurphy2006RiddleHafnerAlexanderampJaeger2000)Drasticchangesinprecipitationacrossthepenin-sulaarebelievedtohaveledtoseveralendemicspeciesbecomingeither locally extinct or restricted to small isolated sites such asoases and canyons (Bernardi Ruiz-Campos amp Camarena-Rosales2007WehnckeLoacutepez-MedelliacutenampEzcurra2010)Thismajoreco-logical transition is thought to have most strongly affected spe-ciesdependentonfreshwatersuchasamphibians(Grismer2002)fishes(Bernardietal2007)andmanyplants(LeoacutendelaLuz2014WehnckeampLoacutepez-Medelliacuten2014)However thesessilenatureofplantsrendersthemparticularlysusceptibletotheinfluenceoffine-scaleenvironmentalheterogeneity(Sorketal2016)whichmakesthefloraoftheBajapeninsulaideallysuitedtoexploringtherelativecontributionsofgeographyandecologytowardspecies-specificre-sponsestoaridification

Palms (Arecaceae)areaspecies-rich taxonomicgroupthathaslongbeenconsideredamodelplantfamilyforevolutionaryandeco-logicalstudiesinthetropics(Baconetal2016CouvreurampBaker2013Kisslingetal2012Savolainenetal2006)Althoughpalmsmainlyoccur in tropical andsubtropical climates (TregearRivalampPintaud 2011) a few species can alsobe found in desert regions(Dransfield etal 2008 Tomlinson 2006) Palm populations onthe Baja California peninsula are widely considered to be relictsof historically more widespread and continuous populations thatare now largely confined to sites where permanent water existseitheraboveorbelowtheground(Axelrod1958BaconBakerampSimmons2012Cornett1985abCornettGlenampStewart1986Felgeramp Joyal 1999GrismerampMcGuire 1993) This is reflectedby the fossil recordwhichshowsthatduring the lateCretaceouspalmswerecommonacrossNorthAmericaandextendedmuchfur-therthantheircurrentgeographicdistribution(CouvreurForestampBaker2011Harley2006)Todaytheonlysuitablenaturalhabitats


















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ACKNOWLEDG MENTS



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(b)

Washingtonia Brahea





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ACKNOWLEDG MENTS



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R E FE R E N C E S










































































































































































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(b)

Washingtonia Brahea





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ACKNOWLEDG MENTS



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R E FE R E N C E S



























































































































































(a) (b)












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(a)

(b)

Washingtonia Brahea





0620 0267 0248 minus0160


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ACKNOWLEDG MENTS



None declared






ORCID




R E FE R E N C E S






























































































































































(a) (b)







(a)

(b)

Washingtonia Brahea





0620 0267 0248 minus0160


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ACKNOWLEDG MENTS



None declared






ORCID




R E FE R E N C E S

























































































































































(a)

(b)

Washingtonia Brahea





0620 0267 0248 minus0160


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ACKNOWLEDG MENTS



None declared






ORCID




R E FE R E N C E S





















































































































































































ACKNOWLEDG MENTS



None declared






ORCID




R E FE R E N C E S



















































































































































genotyping by sequencing reveals contrasting patterns of ...€¦ · ecology and evolution....

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