Strong genetic subdivision in Leptobrachium hendricksoni (Anura: Megophryidae) in Southeast Asia

in Amphibia-Reptilia
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Many biodiversity hotspots are located in areas with a complex geological history, like Southeast Asia, where species diversity may still be far underestimated, especially in morphologically conservative groups like amphibians. Recent phylogenetic studies on the frog genus Leptobrachium from Southeast Asia revealed the presence of deeply divergent mitochondrial clades in Leptobrachium hendricksoni from Malaysia and Sumatra but populations from Thailand have not been studied so far. In this study, we re-evaluate patterns of intraspecific genetic diversity in L. hendricksoni based on the analysis of combined sequences of mitochondrial 12S and 16S genes (1310 base pairs) including for the first time samples from southern Thailand. Thai populations of L. hendricksoni formed a distinct clade with respect to populations from central and southern Malaysia and Sumatra. High sequence divergence between lineages from Thailand, Malaysia and Sumatra suggests the possible presence of cryptic species in L. hendricksoni. Divergence within L. hendricksoni dates back to the late Miocene, around 6 Mya, when lineages from Thailand, north Malaysia and Sumatra split from a lineage in south Malaysia, at about the same time as rising sea levels isolated the Thai-Malay peninsula. Subsequent splits took place later in the Pliocene, around 4.5 and 2.6 Mya. Our results highlight the role of geological history in promoting population divergence and speciation.

Strong genetic subdivision in Leptobrachium hendricksoni (Anura: Megophryidae) in Southeast Asia

in Amphibia-Reptilia

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References

AmphibiaWeb (2014): Information on amphibian biology and conservation Berkeley California. http://amphibiaweb.org/ (Accessed 13 January 2017).

ArévaloE.DavisS.K.SitesJ.W.Jr. (1994): Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Syst. Biol. 43: 387-418.

BandeltH.J.ForsterP.RöhlA. (1999): Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37-48.

BrownR.M.FoufopoulosJ.RichardsS.J. (2006a): New species of Platymantis (Amphibia; Anura: Ranidae) from New Britain and redescription of the poorly known Platymantis nexipus. Copeia 2006: 674-695.

BrownR.M.RichardsS.J. (2008): Two new frogs of the genus Platymantis (Anura: Ceratobatrachidae) from the Isabel Island group, Solomon Islands. Zootaxa 1888: 47-68.

BrownR.M.RichardsS.J.SukumaranJ.FoufopoulosJ. (2006b): A new morphologically cryptic species of forest frog (genus Platymantis) from New Britain Island, Bismarck Archipelago. Zootaxa 1334: 45-68.

BrownR.M.SilerC.D.DiesmosA.C.AlcalaA.C. (2009): Philippine frogs of the genus Leptobrachium (Anura; Megophryidae): phylogeny-based species delimitation, taxonomic review, and descriptions of three new species. Herpetol. Monogr. 23: 1-44.

CabeP.R.PageR.B.HanlonT.J.AldrichM.E.ConnorsL.MarshD.M. (2007): Fine-scale population differentiation and gene flow in a terrestrial salamander (Plethodon cinereus) living in a continuous habitat. Heredity 98: 53-60.

CannatellaD.C.HillisD.M.ChippindaleP.T.WeghtL.RandA.S.RyanM.J. (1998): Phylogeny of frogs of the Physalaemus pustulosus species group, with an examination of data incongruence. Syst. Biol. 47: 311-335.

CannonC.H.MorleyR.J.BushA.B.G. (2009): The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proc. Natl. Acad. Sci. U.S.A. 106: 11188-11193.

CollinsF.H.MendezM.A.RasmussenM.O.BesanskyN.J.FinnertyV. (1987): A ribosomal RNA gene probe differentiates member species of the Anopheles gambiae complex. Am. J. Trop. Med. Hyg. 37: 37-41.

CorlettR.T. (2009): The Ecology of Tropical East Asia. Oxford University PressOxford.

DarribaD.TaboadaG.L.DoalloR.PosadaD. (2012): jModelTest version 2: more models, new heuristics and parallel computing. Nat. Methods 9: 772.

DrummondA.J.SuchardM.A.XieD.RambautA. (2012): Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29: 1969-1973.

EvansB.J.BrownR.M.McGuireJ.A.SupriatnaJ.AndayaniN.DiesmosA.C.IskandarD.MelnickD.J.CannatellaD.C. (2003): Phylogenetics of fanged frogs: testing biogeographical hypotheses at the interface of the Asian and Australian faunal zones. Syst. Biol. 52: 794-819.

ExcoffierL.LischerH.E.L. (2010): Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10: 564-567.

FouquetA.GillesA.VencesM.MartyC.BlancM.GemmellN.J. (2007): Underestimation of species richness in Neotropical frogs revealed by mtDNA analyses. PLoS One 2: e1109.

FrostD.R. (2015): Amphibian Species of the World: an Online Reference. Version 6.0. American. Natural History Museum. http://research.amnh.org/vz/herpetology/amphibia/ (Accessed 9 January 2017).

FuY.X. (1997): Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.

García-ParísM.GoodD.A.Parra-OleaG.WakeD.B. (2000): Biodiversity of Costa Rican salamanders: implications of high levels of genetic differentiation and phylogeographic structure for species formation. Proc. Natl. Acad. Sci. U.S.A. 97: 1640-1647.

HallT.A. (1999): BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.

HamidyA.MatsuiM.NishikawaK.BelabutD.M. (2012): Detection of cryptic taxa in Leptobrachium nigrops (Amphibia, Anura, Megophryidae), with description of two new species. Zootaxa 3398: 22-39.

HamidyA.MatsuiM.ShimadaT.NishikawaK.YambunP.SudinA.KusriniM.D.KurniatiH. (2011): Morphological and genetic discordance in two species of bornean Leptobrachium (Amphibia, Anura, Megophryidae). Mol. Phylogenet. Evol. 61: 904-913.

HedgesS.B. (1994): Molecular evidence for the origin of birds. Proc. Natl. Acad. Sci. U.S.A. 91: 2621-2624.

HuelsenbeckJ.P.RonquistF. (2001): MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754-755.

IBM Corporation (2013): IBM SPSS Statistics for Windows Version 22.0. IBM CorporationArmonk, NY.

IngerR.F.StuebingR.B. (1997): A Field Guide to the Frogs of Borneo. Natural History Publications (Borneo)Kota Kinabalu.

IngerR.F.VorisH.K. (2001): The biogeographical relations of the frogs and snakes of Sundaland. J. Biogeogr. 28: 863-891.

KhonsueW.ThirakhuptK. (2001): A checklist of the amphibians in Thailand. Nat. Hist. J. Chulalongkorn Univ. 1: 69-82.

KuramotoM.SatouN.OumiS.KurabayasiA.SumidaM. (2011): Inter- and intraisland divergence in Odorrana ishikawae (Anura, Ranidae) of the Ryukyu Archipelago of Japan, with description of a new species. Zootaxa 2767: 25-40.

LambeckK.ChappellJ. (2001): Sea level change through the last glacial cycle. Science 292: 679-686.

LeaD.W.MartinP.A.PakD.K.SperoH.J. (2002): Reconstructing a 350 ky history of sea level using planktonic Mg/Ca and oxygen isotope records from Cocos Ridge core. Quat. Sci. Rev. 21: 283-293.

LeighJ.W.BryantD. (2015): PopART: full-feature software for haplotype network construction. Methods Ecol. Evol. 6: 1110-1116.

LibradoP.RozasJ. (2009): DnaSP version 5.10.01: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 24: 1451-1452.

Martínez-SolanoI.JockuschE.L.WakeD.B. (2007): Extreme population subdivision throughout a continuous range: phylogeography of Batrachoseps attenuatus (Caudata: Plethodontidae) in western North America. Mol. Ecol. 16: 4335-4355.

MatsuiM.HamidyA.MurphyR.W.KhonsueW.YambunP.ShimadaT.AhmadN.BelabutD.M.JiangJ.P. (2010): Phylogenetic relationships of megophryid frogs of the genus Leptobrachium (Amphibia, Anura) as revealed by mtDNA gene sequences. Mol. Phylogenet. Evol. 56: 259-272.

MatsuiM.ItoH.ShimadaT.OtaH.SaidapurS.K.KhonsueW.Tanaka-UenoT.WuG. (2005): Taxonomic relationships within the pan-oriental narrow-mouth toad Microhyla ornata as revealed by mtDNA analysis (Amphibia, Anura, Microhylidae). Zool. Sci. 22: 489-495.

MatsuiM.ShimadaT.LiuW.-Z.MaryatiM.KhonsueW.OrlovN. (2006): Phylogenetic relationships of oriental torrent frogs in the genus Amolops and its allies (Amphibia, Anura, Ranidae). Mol. Phylogenet. Evol. 38: 659-666.

MatsuiM.NabhitabhataJ.PanhaS. (1999): On Leptobrachium from Thailand with a description of a new species (Anura: Pelobatidae). Jpn. J. Herpetol. 18: 19-29.

MatsuiM.NishikawaK.KhonsueW.PanhaS.NabhitabhataJ. (2001): Allozymic variation in Rana nigrovittata (Amphibia: Anura) within Thailand with special reference to the taxonomic status of R. mortenseni. Nat. Hist. J. Chulalongkorn Univ. 1: 15-22.

NeiM. (1987): Molecular Evolutionary Genetics. Columbia University PressNew York.

NeiM.TajimaF. (1981): DNA polymorphism detectable by restriction endonuclease. Genetics 97: 145-163.

PfrenderM.E.HicksJ.LynchM. (2004): Biogeographic patterns and current distribution of molecular-genetic variation among populations of speckled dace, Rhinichthys osculus (Girard). Mol. Phylogenet. Evol. 30: 490-502.

RambautA.SuchardM.A.XieD.DrummondA.J. (2014): Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer (Accessed 2 June 2017).

RaoD.Q.WilkinsonJ.A. (2008): Phylogenetic relationships of the mustache toads inferred from mtDNA sequences. Mol. Phylogenet. Evol. 46: 61-73.

RohlingE.J.FentonM.JorissenF.J.BertrandP.GanssenG.CauletJ.P. (1998): Magnitudes of sea-level lowstands of the past 500,000 years. Nature 394: 162-165.

RonquistF.HuelsenbeckJ.P. (2003): MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.

SathiamurthyE.VorisH.K. (2006): Maps of Holocene sea level transgression and submerged lakes on the sunda shelf. Nat. Hist. J. Chulalongkorn Univ. 2 (Suppl.): 1-44.

SenguptaS.ChoudhuryN.K.DasI. (2001): Leptobrachium smithi Matsui, Nabitabhata, and Panha, 1999 (Anura: Megophryidae), a new record for India. J. Bombay Nat. Hist. Soc. 98: 289-290.

SmithC.HeyneS.RichterA.S.WillS.BackofenR. (2010): Freiburg RNA tools: a web server integrating IntaRNA, ExpaRNA and LocARNA. Nucleic Acids Res. 38 (Suppl.): W373-W377.

SondhiS.OhlerA. (2011): A blue-eyed Leptobrachium (Anura: Megophryidae) from Arunachal Pradesh, India. Zootaxa 2912: 28-36.

StuartB.L.IngerR.F.VorisH.K. (2006): High level of cryptic species diversity revealed by sympatric lineages of southeast Asian forest frogs. Biol. Lett. 2006: 470-474.

StuartB.L.PhimmachakS.SeateunS.SivongxayN. (2012): A new Leptobrachium (Anura: Megophryidae) from the highlands of southern Laos. Zootaxa 3155: 29-37.

StuartB.L.RowleyJ.L.TranD.T.A.LeD.T.T.HoangU.D. (2011): The Leptobrachium (Anura: Megophryidae) of the Langbian Plateau, southern Vietnam, with description of a new species. Zootaxa 2804: 25-40.

TajimaF. (1989): Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.

TamuraK.StecherG.PetersonD.FilipskiA.KumarS. (2013): MEGA6: molecular evolutionary genetics analysis version 6.06. Mol. Biol. Evol. 30: 2725-2729.

TaylorE.H. (1962): The amphibian fauna of Thailand. Kans. Univ. Sci. Bull. 63: 265-599.

TominagaA.MatsuiM.NishikawaK.TanabeS. (2006): Phylogenetic relationships of Hynobius naevius (Amphibia: Caudata) as revealed by mitochondrial 12S and 16S rRNA genes. Mol. Phylogenet. Evol. 38: 677-684.

WhitmoreT.C. (1998): An Introduction to Tropical Rain Forests. Oxford University PressOxford.

WillS.ReicheK.HofackerI.L.StadlerP.F.BackofenR. (2012): LocARNA-P: accurate boundary prediction and improved detection of structural RNAs. RNA 18: 900-914.

WillS.ReicheK.HofackerI.L.StadlerP.F.BackofenR. (2007): Inferring non-coding RNA families and classes by means of genome-scale structure-based clustering. PLoS Comput. Biol. 3: e65.

WoganG.O.U. (2012): A new species of Leptobrachium from Myanmar (Anura: Megophryidae). Zootaxa 3415: 23-36.

WoodruffD.S. (2003): Neogene marine transgressions, paleogeography and biogeographic transitions on the Thai-Malay Peninsula. J. Biogeogr. 30: 551-567.

WoodruffD.S. (2010): Biogeography and conservation in Southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today’s patterns and the future of the remaining refugial-phase biodiversity. Biodivers. Conserv. 19: 919-941.

XuQ.LiuS.WanR.YueB.ZhangX. (2014): The complete mitochondrial genome of the Vibrissaphora boringii (Anura: Megophryidae). Mitochondrial DNA A DNA Mapp . Seq. Anal. 27: 758-759.

YodthongS.SilerC.D.PrasankokP.AowpholA. (2014): Phylogenetic patterns of the Southeast Asian tree frog Chiromantis hansenae in Thailand. Asian Herpetol. Res 5: 179-196.

ZhangM.W.RaoD.Q.YangJ.X.YuG.H.WilkinsonJ.A. (2010): Molecular phylogeography and population structure of a mid-elevation montane frog Leptobrachium ailaonnicum in a fragmented habitat of southwest China. Mol. Phylogenet. Evol. 54: 47-58.

ZhengY.C.LiS.Q.FuJ.Z. (2008): A phylogenetic analysis of the frog genera Vibrissaphora and Leptobrachium, and the correlated evolution of nuptial spine and reversed sexual size dimorphism. Mol. Phylogenet. Evol. 46: 695-707.

Figures

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    Map of the Thai-Malay peninsula and Sumatra showing land mass changes through the geological history of the region. Shaded areas represent different land mass extensions when sea level was at (a) 100 m and (b) 25 m above present level in the Miocene and the Pliocene (adopted from Woodruff, 2003), (c) −60 m in the Pleistocene and (d) −120 m below present level in the last glacial period (adopted from Sathiamurthy and Voris, 2006).

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    Map of the Thai-Malay peninsula and Sumatra showing sampling localities of L. hendricksoni. Localities 1-27 were sampled for the present study and localities 28-35 were sampled in previous studies with sequences downloaded from GenBank. Sample codes as in Table 1. The shaded area represents the distribution range of L. hendricksoni in Thailand, Malaysia and Sumatra.

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    Time-calibrated gene tree reconstructed with BEAST, based on the analysis of 1310 bp of combined 12S rRNA and 16S rRNA mitochondrial genes for samples of L. hendricksoni (including the four major lineages discussed) and three outgroups. Sample codes and localities as in Table 1. Numbers on nodes represent ML bootstrap support values and Bayesian posterior probabilities, respectively (ML/BPP). Node ages are represented by horizontal bars (95% highest posterior density intervals) and numbers next to the nodes (median estimates). Scale (bottom) in millions of years.

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    Median joining haplotype network of combined mitochondrial 12S and 16S sequences showing the relationships among haplotypes of L. hendricksoni. Circles represent haplotypes, with sizes proportional to the number of the individuals sharing that haplotype. Hatch marks on the branches represent the number of mutations distinguishing haplotypes.

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