Weak genetic divergence between the two South American toad-headed turtles Mesoclemmys dahli and M. zuliae (Testudines: Pleurodira: Chelidae)

in Amphibia-Reptilia
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Mesoclemmys dahli and M. zuliae are two endangered, little-known toad-headed turtles with small distribution ranges in Colombia and Venezuela, respectively. Using the mitochondrial cytochrome b gene as a marker, we investigate their phylogeographic differentiation. Furthermore, based on 2341 bp of mtDNA and 2109 bp of nDNA of M. dahli, M. zuliae and allied chelid turtles, we infer their divergence time using a fossil-calibrated relaxed molecular clock approach. Mesoclemmys dahli and M. zuliae are closely related species, with an estimated mean divergence time of 10.6 million years. This estimate correlates with the uplift of the Serranía de Perijá, an Andean mountain chain separating their distribution ranges, suggesting that this event could have caused the evolution of the two species. Haplotype and nucleotide diversities of M. dahli are markedly higher than in Podocnemis lewyana, another endemic turtle species of Colombia. This pronounced dissimilarity may reflect differences in the phylogeographies and demographic histories of the two species, but also different habitat preferences.

Weak genetic divergence between the two South American toad-headed turtles Mesoclemmys dahli and M. zuliae (Testudines: Pleurodira: Chelidae)

in Amphibia-Reptilia



AmatoM.L.BrooksR.J.FuJ. (2008): A phylogeographic analysis of populations of the wood turtle (Glyptemys insculpta) throughout its range. Mol. Ecol. 17: 570-581.

BohonakA.J. (2002): IBD (Isolation-by-Distance): a program for analyses of isolation by distance. J. Hered. 93: 153-154.

BourR.ZaherH. (2005): A new species of Mesoclemmys, from the open formations of Northeastern Brazil (Chelonii, Chelidae). Pap. Avul. Zool. 45: 295-311.

ButlerJ.M.DoddC.K.ArescoM.AustinJ.D. (2011): Morphological and molecular evidence indicates that the Gulf Coast box turtle (Terrapene carolina major) is not a distinct evolutionary lineage in the Florida Panhandle. Biol. J. Linn. Soc. 102: 889-901.

CadenaE.A. (2011): Potential earliest record of podocnemidoid turtles from the Early Cretaceous (Valanginian) of Colombia. J. Paleontol. 85: 877-881.

Castaño-MoraO.V.MedemF. (2002): Batrachemys dahli. In: Libro rojo de reptiles de Colombia. Libros rojos de especies amenazadas de Colombia p.  77-79. Castaño-MoraO.V. Ed. Instituto de Ciencias Naturales (Universidad Nacional de Colombia), Ministerio del Medio Ambiente and Conservación InternacionalBogotá, Colombia.

ClementM.PosadaD.CrandallK.A. (2000): TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9: 1657-1660.

de la FuenteM.UmazanoA.M.SterliJ.CarballidoJ.L. (2011): New chelid turtles of the lower section of the Cerro Barcino formation (Aptian-Albian?), Patagonia, Argentina. Cretaceous Res. 32: 527-537.

de la Ossa-VelasquezJ.L. (1998): Phrynops dahli: a little known turtle endemic to the Caribbean coast of Colombia. Reptilia 3: 47-50.

Forero-MedinaG.Cárdenas-ArevaloG.Castaño-MoraO.V. (2011): Abundance, home range, and movement patterns of the endemic species Dahl’s toad-headed turtle (Mesoclemmys dahli) in Cesar, Colombia. Chelon. Conserv. Biol. 10: 228-236.

FritzU.HavašP. (2007): Checklist of chelonians of the world. Vertebr. Zool. 57: 149-368.

FritzU.FattizzoT.GuickingD.TripepiS.PennisiM.G.LenkP.JogerU.WinkM. (2005): A new cryptic species of pond turtle from southern Italy, the hottest spot in the range of the genus Emys. Zool. Scr. 34: 351-371.

FritzU.AuerM.BertoleroA.CheylanM.FattizzoT.HundsdörferA.K.Martín SampayoM.PretusJ.L.ŠirokýP.WinkM. (2006): A rangewide phylogeography of Hermann’s tortoise, Testudo hermanni (Reptilia: Testudines: Testudinidae): implications for taxonomy. Zool. Scr. 35: 531-543.

FritzU.GuickingD.KamiH.ArakelyanM.AuerM.AyazD.Ayres FernándezC.BakievA.G.CelaniA.DžukićG.FahdS.HavašP.JogerU.KhabibullinV.F.MazanaevaL.F.ŠirokýP.TripepiS.Valdeón VélezA.Velo AntónG.WinkM. (2007): Mitochondrial phylogeography of European pond turtles (Emys orbicularis, Emys trinacris) – an update. Amphib.-Reptil. 28: 418-426.

FritzU.AyazD.BuschbomJ.KamiH.G.MazanaevaL.F.AloufiA.A.AuerM.RifaiL.ŠilićT.HundsdörferA.K. (2008): Go east: phylogeographies of Mauremys caspica and M. rivulata – discordance of morphology, mitochondrial and nuclear genomic markers and rare hybridization. J. Evolution. Biol. 21: 527-540.

FritzU.AyazD.HundsdörferA.K.KotenkoT.GuickingD.WinkM.TokC.V.ÇiçekK.BuschbomJ. (2009): Mitochondrial diversity of European pond turtles (Emys orbicularis) in Anatolia and the Ponto-Caspian Region: multiple old refuges, hotspot of extant diversification and critically endangered endemics. Org. Divers. Evol. 9: 100-114.

FritzU.AlcaldeL.Vargas-RamírezM.GoodeE.V.Fabius-TuroblinD.U.PraschagP. (2012a): Northern genetic richness and southern purity, but just one species in the Chelonoidis chilensis complex. Zool. Scr. 41: 220-232.

FritzU.StuckasH.Vargas-RamírezM.HundsdörferA.K.MaranJ.PäckertM. (2012b): Molecular phylogeny of Central and South American slider turtles: implications for biogeography and systematics (Testudines: Emydidae: Trachemys). J. Zool. Syst. Evol. Res. 50: 125-136.

FujitaM.F.EngstromT.N.StarkeyD.E.ShafferH.B. (2004): Turtle phylogeny: insights from a novel nuclear intron. Mol. Phylogenet. Evol. 31: 1031-1040.

GaffneyE.S.TongH.MeylanP.A. (2006): Evolution of the side-necked turtles: the families Bothremydidae, Euraxemydidae, and Araripemydidae. Bull. Am. Mus. Nat. Hist. 300: 1-700.

GeorgesA.BirrelJ.SaintK.M.McCordW.P.DonnellanS.C. (1998): A phylogeny for side-necked turtles (Chelonia: Pleurodira) based on mitochondrial and nuclear gene sequence variation. Biol. J. Linn. Soc. 67: 213-246.

González-PorterG.P.HailerF.Flores-VillelaO.García-AnleuR.MaldonadoJ.E. (2011): Patterns of genetic diversity in the critically endangered Central American river turtle: human influence since the Mayan age? Conserv. Genet. 12: 1229-1242.

HallT.A. (1999): BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 4: 95-98.

HebertP.D.N.RatnasinghamS.de WaardJ.R. (2003): Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc. R. Soc. Lond. B 270: S96-S99.

IUCN [International Union for the Conservation of Nature and Natural Resources] (2011): IUCN Red List of Threatened Species 2011.2. http://www.iucnredlist.org [accessed 22 February 2012].

KarlS.A.WilsonD.S. (2001): Phylogeography and systematics of the mud turtle, Kinosternon baurii. Copeia 2001: 797-801.

KelloggJ.N. (1984): Cenozoic tectonic history of the Sierra de Perijá, Venezuela-Colombia, and adjacent basins. Geol. Soc. Am. Mem. 162: 239-261.

KindlerC.BranchW.R.HofmeyrM.D.MaranJ.ŠirokýP.VencesM.HarveyJ.HauswaldtJ.S.SchleicherA.StuckasH.FritzU. (2012): Molecular phylogeny of African hinge-back tortoises (Kinixys): implications for phylogeography and taxonomy (Testudines: Testudinidae). J. Zool. Syst. Evol. Res. 50: 192-201.

KocherT.D.ThomasW.K.MeyerA.EdwardsS.V.PääboS.VillablancaF.X.WilsonA.C. (1989): Dynamics of mitochondrial DNA evolution in mammals: amplification and sequencing with conserved primers. PNAS 86: 6196-6200.

LambT.LydeardC.WalkerR.B.GibbonsJ.W. (1994): Molecular systematics of map turtles (Graptemys): a comparison of mitochondrial restriction site versus sequence data. Syst. Biol. 43: 543-559.

LeM.RaxworthyC.J.McCordW.P.MertzL. (2006): A molecular phylogeny of tortoises (Testudines: Testudinidae) based on mitochondrial and nuclear genes. Mol. Phylogenet. Evol. 40: 517-531.

LenkP.FritzU.JogerU.WinkM. (1999): Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758). Mol. Ecol. 8: 1911-1922.

LiC.WuX.-C.RieppelO.WangL.-T.ZhaoL.-J. (2008): An ancestral turtle from the Late Triassic of southwestern China. Nature 456: 497-501.

LibradoP.RozasJ. (2009): DNASP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.

McGaughS.E.EckermanC.M.JanzenF.J. (2008): Molecular phylogeography of Apalone spinifera. Zool. Scr. 37: 289-304.

MedemF. (1966): Contribuciones al conocimiento sobre la ecología y distribución geográfica de Phrynops (Batrachemys) dahli (Testudinata, Pleurodira, Chelidae). Caldasia 9: 467-489.

Medina-RangelG.F.Forero-MedinaG.A. (2008): Geographical distribution. Mesoclemmys dahli. Herpetol. Rev. 39: 366.

NylanderJ.A.A. (2002): MrMODELTEST v1.0b. Program distributed by the author. Available from: http://www.ebc.uu.se/systzoo/staff/nylander.html [accessed 22 February 2012].

NylanderJ.A.A.RonquistF.HuelsenbeckJ.P.Nieves-AldreyJ.L. (2004): Bayesian phylogenetic analysis of combined data. Syst. Biol. 53: 47-67.

PearseD.E.ArndtA.D.ValenzuelaN.MillerB.A.CantarelliV.SitesJ.R. (2006): Estimating population structure under nonequilibrium conditions in a conservation context: continent-wide population genetics of the giant Amazon River turtle, Podocnemis expansa (Chelonia; Podocnemididae). Mol. Ecol. 15: 985-1006.

PedallI.FritzU.StuckasH.ValdéonA.WinkM. (2011): Gene flow across secondary contact zones of the Emys orbicularis complex in the Western Mediterranean and evidence for extinction and re-introduction of pond turtles on Corsica and Sardinia (Testudines: Emydidae). J. Zool. Syst. Evol. Res. 49: 44-57.

PraschagP.HundsdörferA.K.FritzU. (2007): Phylogeny and taxonomy of endangered South and South-east Asian freshwater turtles elucidated by mtDNA sequence variation (Testudines: Geoemydidae: Batagur, Callagur, Hardella, Kachuga, Pangshura). Zool. Scr. 36: 429-442.

PraschagP.StuckasH.PäckertM.MaranJ.FritzU. (2011): Mitochondrial DNA sequences suggest a revised taxonomy of Asian flapshell turtles (Lissemys Smith, 1931) and the validity of previously unrecognized taxa (Testudines: Trionychidae). Vertebr. Zool. 61: 147-160.

PritchardP.C.H.TrebbauP. (1984): The Turtles of Venezuela. Contributions to Herpetology 2. Society for the Study of Amphibians and ReptilesOxford, Ohio.

Rojas-RunjaicF.J.M. (2009): Mesoclemmys zuliae, el enigmático galápago “cabezón” del sur del lago Maracaibo. Reptilia 80: 31-38.

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

RosenbaumP.A.RobertsonJ.A.ZamudioK.R. (2007): Unexpectedly low genetic divergences among populations of the threatened bog turtle (Glyptemys muhlenbergii). Conserv. Genet. 8: 331-342.

Rueda-AlmonacidJ.V.CarrJ.L.MittermeierR.A.Rodríguez-MahechaJ.V.MastR.B.VogtR.C.RhodinA.G.J.de la Ossa-VelásquezJ.RuedaJ.N.Goettsch-MittermeierC. (2007): Las Tortugas y los cocodrilianos de los países andinos del trópico. Bogotá Conservación Internacional (Serie de guías tropicales de campo).

SilvestroD.MichalakI. (2011): raxmlGUI: a graphical frontend for RAxML. Org. Divers. Evol. DOI:10.1007/s13127-011-0056-0.

SouzaF.L. (2005): Geographical distribution patterns of South American side-necked turtles (Chelidae), with emphasis on Brazilian species. Rev. Esp. Herpetol. 19: 33-46.

SouzaF.L.CunhaA.F.OliveiraM.A.PereiraG.A.G.dos ReisS.F. (2003): Preliminary phylogeographic analysis of the Neotropical freshwater turtle Hydromedusa maximiliani (Chelidae). J. Herpetol. 37: 427-433.

StamatakisA. (2006): RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.

StuartB.L.ParhamJ.F. (2004): Molecular phylogeny of the critically endangered Indochinese box turtle (Cuora galbinifrons). Mol. Phylogenet. Evol. 31: 164-177.

StuckasH.FritzU. (2011): Identity of Pelodiscus sinensis revealed by DNA sequences of an approximately 180-year-old type specimen and a taxonomic reappraisal of Pelodiscus species (Testudines: Trionychidae). J. Zool. Syst. Evol. Res. 49: 335-339.

TamuraK.PetersonD.PetersonN.StecherG.NeiM.KumarS. (2011): MEGA 5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.

ThorneJ.L.KishinoH. (2002): Divergence time and evolutionary rate estimation with multilocus data. Syst. Biol. 51: 689-702.

ThorneJ.L.KishinoH.PainterI.S. (1998): Estimating the rate of evolution of the rate of molecular evolution. Mol. Biol. Evol. 15: 1647-1657.

Ureña-ArandaC.A.Espinosa de los MonterosA. (2012): The genetic crisis of the Mexican Bolson tortoise (Gopherus flavomarginatus: Testudinidae). Amphib.-Reptil. 33: 45-53.

van DijkP.P.IversonJ.B.ShafferH.B.BourR.RhodinA.G.J. (2011): Turtles of the world, 2011 update: annotated checklist of taxonomy, synonymy, distribution, and conservation status. Chelon. Res. Monogr. 5: 000.165-000.242.

Vargas-RamírezM.ChiariY.Castaño-MoraO.V.MenkenS.B.J. (2007): Low genetic variability in the endangered Colombian endemic freshwater turtle Podocnemis lewyana (Testudines, Podocnemididae). Contr. Zool. 76: 1-7.

Vargas-RamírezM.MaranJ.FritzU. (2010a): Red- and yellow-footed tortoises (Chelonoidis carbonaria, C. denticulata) in South American savannahs and forests: do their phylogeographies reflect distinct habitats? Org. Divers. Evol. 10: 161-172.

Vargas-RamírezM.VencesM.BranchW.R.DanielsS.R.GlawF.HofmeyrM.D.KuchlingG.MaranJ.PapenfussT.J.ŠirokýP.VieitesD.R.FritzU. (2010b): Deep genealogical lineages in the widely distributed African helmeted terrapin: evidence from mitochondrial and nuclear DNA (Testudines: Pelomedusidae: Pelomedusa subrufa). Mol. Phylogenet. Evol. 56: 428-440.

Vargas-RamírezM.StuckasH.Castaño-MoraO.V.FritzU. (2012): Extremely low genetic diversity and weak population differentiation in the endangered Colombian river turtle Podocnemis lewyana (Testudines: Podocnemididae). Conserv. Genet. 13: 65-77.

WalkerD.MolerP.E.BuhlmannK.A.AviseJ.C. (1998): Phylogeographic uniformity in mitochondrial DNA of the snapping turtle (Chelydra serpentina). Anim. Conserv. 1: 55-60.

WeisrockD.W.JanzenF.J. (2000): Comparative molecular phylogeography of North American softshell turtles (Apalone): implications for regional and wide-scale historical evolutionary forces. Mol. Phylogenet. Evol. 14: 152-164.

YangZ. (1997): PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13: 555-556.

ZangerlR.MedemF. (1958): A new species of chelid turtle, Phrynops (Batrachemys) dahli, from Colombia. Bull. Mus. Comp. Zool. 119: 373-390.


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    Distribution of Mesoclemmys dahli and M. zuliae (based on Rueda-Almonacid et al., 2007) and sampling sites (colour-coded). For M. dahli, the Córdoba population is indicated in green and the Cesar population in orange; sites of M. zuliae, blue. The Serranía de Perijá is highlighted in red. Inset: juvenile Mesoclemmys dahli from the Cesar population (photo: Guido Medina).

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    Parsimony network of cyt b haplotypes of Mesoclemmys dahli and M. zuliae, based on an alignment of 1067 bp length. Circle size indicates haplotype frequency. Missing haplotypes are shown as small black circles. Each line connecting haplotypes corresponds to one mutational step. Colour code as in fig. 1; haplotype codes refer to the Appendix.

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    Bayesian tree based on 2341 bp of mitochondrial DNA (12 S rRNA, ND4, cyt b) and 2109 bp of nuclear DNA sequences (C-mos, R35, Rag 2; partitioned by gene). Support values are Bayesian posterior probabilities (top) and ML bootstrap values (bottom); asterisks indicate maximum support under both methods. This tree was used for the Relaxed Molecular Clock calculations.

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    Divergence time estimates using the MULTIDISTRIBUTE package. Dark grey bars at nodes represent 95% confidence intervals. The light grey column on the right shows the time of the main uplift of the Serranía de Perijá (Late Miocene-Pliocene; Kellogg, 1984). Letters indicate nodes calibrated with fossil evidence (see table 1). PP, Plio-Pleistocene.


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