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BMC Evolutionary Biology This Provisional PDF corresponds to the article as it appeared upon acceptance. Fully formatted PDF and full text (HTML) versions will be made available soon. Toad radiation reveals into-India dispersal as a source of endemism in the Western Ghats-Sri Lanka biodiversity hotspot BMC Evolutionary Biology 2009, 9:131 doi:10.1186/1471-2148-9-131 Ines Van Bocxlaer ([email protected]) S D Biju ([email protected]) Simon P Loader ([email protected]) Franky Bossuyt ([email protected]) ISSN 1471-2148 Article type Research article Submission date 29 October 2008 Acceptance date 11 June 2009 Publication date 11 June 2009 Article URL http://www.biomedcentral.com/1471-2148/9/131 Like all articles in BMC journals, this peer-reviewed article was published immediately upon acceptance. It can be downloaded, printed and distributed freely for any purposes (see copyright notice below). Articles in BMC journals are listed in PubMed and archived at PubMed Central. For information about publishing your research in BMC journals or any BioMed Central journal, go to http://www.biomedcentral.com/info/authors/ © 2009 Van Bocxlaer et al. , licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Toadradiationrevealsinto-Indiadispersalasasourceofendemismin theWesternGhats-SriLankabiodiversityhotspot InesVanBocxlaer1,S.D.Biju2,SimonP.Loader3andFrankyBossuyt1* Address: 1AmphibianEvolutionLab,BiologyDepartment,UnitofEcology&Systematics,Vrije UniversiteitBrussel(VUB),Pleinlaan2,B-1050Brussels,Belgium 2 Systematics Lab, Centre for Environmental Management of Degraded Ecosystems (CEMDE),SchoolofEnvironmentalStudies,UniversityofDelhi110007,India 3InstituteofBiogeography,DepartmentofEnvironmentalSciences,UniversityofBasel, Klingelbergstrasse27,4056Basel,Switzerland. Email: Ines Van Bocxlaer - [email protected]; S.D. Biju - [email protected]; [email protected];[email protected] *Correspondingauthor 1 Abstract Background: High taxonomic level endemism in the Western Ghats-Sri Lanka biodiversityhotspothasbeentypicallyattributedtothesubcontinent'sgeologicalhistory of long-term isolation. Subsequent out of - and into India dispersal of species after accretiontotheEurasianmainlandisthereforeoftenseenasabiogeographicfactorthat ‘diluted’ the composition of previously isolated Indian biota. However, few molecular studies have focussed on into-India dispersal as a possible source of endemism on the subcontinent. Using c. 6000 base pairs of mitochondrial and nuclear DNA, we investigatedtheevolutionaryhistoryandbiogeographyoftruetoads(Bufonidae),agroup thatcolonizedtheIndianSubcontinentaftertheIndo-Asiacollision. Results:Contrarytopreviousstudies,OldWorldtoadswererecoveredasanestedclade withinNewWorldBufonidae,indicatingasinglecolonizationevent.Speciescurrently classified as Ansonia and Pedostibes were both recovered as being non-monophyletic, providingevidencefortheindependentoriginoftorrentialandarborealecomorphsonthe Indian subcontinent and in South-East Asia. Our analyses also revealed a previously unrecognized adaptive radiation of toads containing a variety of larval and adult ecomorphs.Moleculardatingestimatesandbiogeographicanalysesindicatethattheearly diversificationofthiscladehappenedintheWesternGhatsandSriLankaduringtheLate OligocenetoEarlyMiocene. Conclusion: PaleoclimatereconstructionshaveshownthattheEarlyNeogeneof India was marked by major environmental changes, with the transition from a zonal- to the current monsoon-dominated climate. After arrival in the Western Ghats-Sri Lanka hotspot,toadsdiversifiedinsitu,withonlyonelineageabletosuccessfullydisperseout 2 of these mountains. Consequently, higher taxonomic level endemism on the Indian SubcontinentisnotonlytheresultofCretaceousisolation,butalsoofinvasion,isolation andradiationofnewelementsafteraccretiontotheEurasianmainland. 3 Background TheWesternGhatsof IndiaandhighlandsofSri Lankaarea global biodiversity hotspot,i.e.theycontainseveralendemicanimalandplantspecieswhicharerecognised asbeingdistinctatahightaxonomiclevel[1].Endemismisparticularlymarkedamong amphibians,withover75%ofsubcontinentspeciesrestrictedtothisregionalone[2,3]. Explainingbiogeographicpatternshasmainlyfocussedonthegeologicalhistoryofthe subcontinent,whichindicatesprolongedperiodsofisolationfromtheLateCretaceousto the Early Tertiary [4-9]. Before joining the Eurasian mainland, India was part of Gondwana (South-America, Africa, Indo-Madagascar, Australia-New Guinea and Antarctica)andgraduallybecamedetachedfromotherlandmassesduringitsnorthward journeyacrosstheTethysSea [10-12]. Althoughtheactualisolation of Indiahasbeen debated (see [13] and references therein), molecular studies have demonstrated the presence of ancient lineages in India, and these are interpreted as evidence of this geologicalhistory[4-6]. ThesubsequentaccretionoftheIndianplateintoEurasiaduringtheEarlyTertiary [13] was a potential catalyst for biotic exchange between the subcontinent and the Eurasian mainland. It has been shown that an out-of-India dispersal of Gondwanan elementsintoEurasiaresultedinthewiderdistributionofpreviouslyisolatedgroups[5, 14-17]. However, less attention has been given to the opportunity of "into-India" movementofLaurasianspeciesaftertheestablishmentofthisnewgeologicalconnection. TheexchangeofspeciesbetweentheIndianSubcontinentandEurasiamusthavebeen affectedbythegeomorphologicalchangesgeneratedaftertheircollision.Theupliftofthe HimalayasandtheTibetanPlateaunotonlycreatedphysicalbarriersfordispersal,but also heavily influenced the prevalent climate [18, 19]. The climatic regime in Asia 4 changedfromazonal-patterntoamonsoon-dominantsystem,areorganizationthathad majorconsequencesforAsianandIndianterrestrialecosystems[20,21]. Truetoads(Bufonidae)areafamilyofanuranswithawidedistribution,comprising over 500 species [22, 23]. Their present-day natural absence on several landmasses of Gondwanan origin (Australia, Madagascar, Seychelles), their nested position within Nobleobatrachia (Hyloidea sensu [6]), and their recent origin [24-26], imply that they reachedtheIndiansubcontinentonlyaftertheIndo-Asiacollision.Toadsthusconstitute an ideal group for studying Tertiary into-India dispersal. Despite numerous studies on phylogenetic relationships in Bufonidae [27-38], species from the Indian subcontinent were always underrepresented and their phylogenetic relationships remain largely elusive.Inadditiontomultiplespecieswhosetaxonomicaffiliationsareuncertain(i.e., provisionallylabelled"Bufo"pendingmoredetailedphylogeneticevidence[37]),toads on the Indian subcontinent are classified in five genera: Bufoides (North-India) and Adenomus(SriLanka)areconsideredendemictothesubcontinent,Duttaphrynushasa widedistribution,andtorrentiallyadaptedAnsoniaandarborealPedostibesspeciesshow disjunct distributions in wet–zone areas of South-East Asia and India [23]. Current taxonomythereforesuggestsmultipledispersaleventsbetweentheIndiansubcontinent andadjacentregions. Hereweanalysedacombinedsetofmitochondrialandnucleargenefragmentsto investigate phylogenetic relationships and biogeography of Indian Bufonidae. Our sampling includes 15 toads from the subcontinent and a representative diversity of species of adjacent regions, with particular attention to shared genera Ansonia, Pedostibes and Duttaphrynus. We performed dating estimates and biogeographic analyses to investigate biotic exchange between the Indian subcontinent and adjacent 5 regions, and evaluated how this affected endemism in the Western Ghats-Sri Lanka biodiversityhotspot. ResultsandDiscussion PhylogeneticrelationshipsofBufonidae Ourdatamatrixconsistsof6309basepairs(bp,4339bpmitochondrial-and1970 bp nuclear DNA), 5116 bp of which could be unambiguously aligned. Maximum Parsimony(MP)analysesofthetotaldatasetproduced2equallyparsimonioustreesof 15224steps.Maximumlikelihood(ML)analysesofthetotaldatasetproducedasingle MLtree(-lnL=71238.66624,withgammashapeparameter=0.533,andproportionof invariable sites = 0.483), which is very similar to the Bayesian consensus phylogram (Figure1). Ouranalysesconfidentlydeterminethephylogeneticpositionoftenknown species currently treated as incertae sedis (“Bufo” in Figure 1). In agreement with previousevidence[31,32],werecoverwithhighsupporttheNorthernAfrican“Bufo” mauritanicusassisterspeciesofasub-SaharanAmietophrynusclade(Figure1).Basedon thissupport,wesuggesttransferringthespecies"Bufo"mauritanicusSchlegel,1841to the genus Amietophrynus. The remaining "Bufo" species in our study are nested in, or closelyrelatedtothegenusDuttaphrynusasoriginallydefined([37],i.e.inessencethe Bufomelanostictusgroupsensulato[39,40],Table1).TheBufoscabergroup[39],here represented by “Bufo” scaber and “Bufo” atukoralei, is nested in Duttaphrynus. To restoremonophylyofDuttaphrynusandtoplacesampled“Bufo”speciesinataxonomic framework, we suggest expanding Duttaphrynus to include the most recent common ancestorofBufomelanostictus(Schneider,1799)andBufostomaticusLütken,1864,and all of its descendants. Eight known species, including those belonging to the Bufo 6 stomaticusgroup sensu [39] (hererepresentedby “Bufo”dhufarensis,“Bufo”hololius and“Bufo”stomaticus),arethustransferredtothisgenus(Figure1,2). Incontrasttopreviousstudies,werecoverwithhighsupporttheOldWorldtoadsas a clade
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