Conservation Genetics

, Volume 12, Issue 5, pp 1229–1242 | Cite as

Patterns of genetic diversity in the critically endangered Central American river turtle: human influence since the Mayan age?

  • Gracia P. González-Porter
  • Frank Hailer
  • Oscar Flores-Villela
  • Rony García-Anleu
  • Jesús E. Maldonado
Research Article


We conducted a phylogeographic analysis of the strictly aquatic and critically endangered Central American river turtle, Dermatemys mawii, as part of a conservation management program for the species. We sampled 238 individuals from 15 different localities throughout the species range. Using sequence fragments from the mtDNA Cyt b and ND4 genes, we identified 16 different haplotypes. Overall, our results reveal a signal of phylogeographic structure throughout the range, which appears to have been secondarily blurred by extensive gene flow. Notably, this also applies to genetic structuring across three major hydrological basins that pose biogeographic breaks in other aquatic taxa. Divergence times of mtDNA haplotypes in D. mawii suggest that the main lineages split in the Pliocene–Pleistocene (3.73–0.227 MA) and demographic tests indicate that the species has undergone drastic demographic size fluctuations since this time period. One ancient haplotype (1D) was found to exhibit sequence divergence of up to 2% from other haplogroups. Divergence of this magnitude is indicative of species level differentiation in other turtle genera. Haplotype 1D was found in only two localities, Sarstun and Salinas, but specimens with other haplotypes were also found in those localities. It is not known whether the individuals with the 1D haplotype interbreed with non-1D individuals. Our results suggest that human activity, such as harvesting and long distance transport of animals, may have influenced the current patterns of genetic diversity. For more than 2000 years, D. mawii has been consumed by people from Middle American cultures, and the archeological record contains strong evidence that the Mayans transported animals between villages and far away from their natural distribution range. Therefore, the large-scale pattern of haplotype sharing even across hydrological barriers, the observed low haplotype diversity in some populations and the contemporary absence of a pronounced phylogeographic pattern is likely due to a combination of population expansions, gene flow, extensive human-mediated-movements and recent bottlenecks resulting from over-harvesting.


Population genetic structure Dermatemys mawii Dermatemydidae Mitochondrial DNA Freshwater turtles 



We thank the Posgrado en Ciencias Biologicas from Universidad Nacional Autonoma de Mexico UNAM; Drs. Ella Vazquez and Luis Medrano Gonzalez for their valuable insights into the experimental design and data analysis which greatly improved the quality of this manuscript. Funding was provided by Consejo Nacional de Ciencia y Tecnología (CONACYT) fellowship No. 210994; the Turtle Conservation Fund grants in 2004, 2006 and 2009; Conservation International grants in 2007, and 2009; the Philadelphia Zoo Conservation Program Financial Support for 2005, 2006, 2007, 2008, an award from the Philadelphia Zoo Docent council in 2007 and Elizabeth A. Schreiber and Seabird Research, Inc. We are grateful to Robert C. Fleischer and Nancy Rotzel for funding and laboratory support at the SCBI’s Center for Conservation and Evolutionary Genetics. To Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT) for the collection permits: SGPA/DGVS/11385/04; SGPA/DGVS/01789/06 to CITES for permits: MX 23732/05; MX 25219/05; MX29137/06; GT175507; MX42603/08; to the government of Belize for permit No. 3176/08; to the USFWS for permits #MA095827-0; MA119634-0/06; MA139456-0/07; MA194812-0/08; EN/FIS/15/04/08(10)Vol1. To SEMARNAT and Procuraduría Federal de Protección al Ambiente (PROFEPA) in Veracruz, and Tabasco. Thanks to all the people who have helped on different parts of this project; for ideas: Miriam Tsuchiya Jerep, for her important help on running the program BEAST, K. Buhlmann and Peter Paul Van Dijk; special thanks to Richard C. Vogt, who help me consolidate the idea of this project and sharing his expertise on the species. Dr. John Polisar, Carlina Peña, Rene Calderon, Humberto Bahena, Matha Vaca, Raul Rodriguez, Lisette Ramos, Greg Georges, Sam Rivera, Judith Rangel, Erasmo Cazares, Darwin Jimenez, Samuel Cabrera, Kenia Laparra, Manuel Acevedo, Claudia Zenteno, and Filiberto Ascencio Jimenez, the staff from WCS in Flores, Guatemala, all the volunteers, and staff at the turtle farm in Nacajuca, Tabasco, and Zoologico Yumka, Fishermen Cooperative of La Union in Quintana Roo for their help in the collection and measuring of the animals. Thanks also to Basilio Sanchez Luna, Gregorio de la Cruz López, and Sharon Matola for allowing us to work with the animals at their facilities, and to Dr. Jonathan Campbell and Carl Franklin from the Amphibian and Reptile Diversity Research Center of the University of Texas at Arlington for the donation of turtle samples for this study, to Joseph R Mendelson, for the information on Phylogeography of the genus Bufo, and to three anonymous reviewers whose comments greatly enhanced the quality of this manuscript.


  1. Aguirre G (2007) Mexico, Conservation of the Central American river turtle in Veracruz. Turtle Survival Alliance, 24–25 AugustGoogle Scholar
  2. Allard MW, Miyamoto MM, Bjorndal KA, Bolton AB, Bowen BW (1994) Support for natal homing in green turtles from mitochondrial DNA sequences. Copeia 1:34–41CrossRefGoogle Scholar
  3. Arbogast BS, Edwards SV, Wakeley J, Beerli P, Slowinski J (2002) Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Annu Rev Ecol Syst 33:707–740CrossRefGoogle Scholar
  4. Avise JC, Bowen BW, Lamb T, Meylan AB, Bermingham E (1992) Mitochondrial DNA evolution at turtle’s pace for genetic variability and reduced microevolutionary rate in the Testudines. Mol Biol Evol 9:457–473PubMedGoogle Scholar
  5. Bickham JW (1981) Two-hundred-million-years-old chromosomes: deceleration of the rate of karyotypic evolution in turtles. Science 212:1291–1293PubMedCrossRefGoogle Scholar
  6. Bickham JW, Carr JL (1983) Taxonomy and phylogeny of the higher categories of Cryptodiran turtles based on a cladistic analysis of chromosomal data. Copeia 4:918–932CrossRefGoogle Scholar
  7. Bowen BW, Meylan AB, Ross JP, Limpus CJ, Balazs GH, Avise JC (1992) Global population structure and natural history of the green turtle (Chelonia mydas) in terms of matriarchal phylogeny. Evolution 46:865–881CrossRefGoogle Scholar
  8. Bowen BW, Nelson WS, Avise JC (1993) A molecular phylogeny for marine turtles: trait mapping, rate assessment, and conservation relevance. Proc Natl Acad Sci USA 90:5574–5577PubMedCrossRefGoogle Scholar
  9. Campbell J (1989) Amphibians and reptiles of northern Guatemala, the Yucatan, and Belize. University of Oklahoma Press, NormanGoogle Scholar
  10. Carrol RL (1988) Vertebrate paleontology and evolution. Freeman, New YorkGoogle Scholar
  11. Castellanos-Cabrera J (2007) Buenavista-Nuevo San José, Petén, Guatemala otra Aldea del Preclásico Medio (800–400 A.C.). FAMSI. Accessed 12 Dec 2009
  12. Clement M, Posada D, Cranall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  13. CONABIO-DGVS-CONANP (2009) Estrategia nacional para la conservación y el manejo sostenible de la Tortuga blanca (Dermatemys mawii) en México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad CONABIO, MéxicoGoogle Scholar
  14. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Tree 15:290–295PubMedGoogle Scholar
  15. Duellmann WE (1966) The Central American herpetofauna: an ecological perspective. Copeia 4:700–719CrossRefGoogle Scholar
  16. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581PubMedCrossRefGoogle Scholar
  17. Edmans S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475CrossRefGoogle Scholar
  18. Elson C, Mowbray K (2005) Burial practices at Teotihuacan in the early postclassic period. The Vaillant and Linne excavations (1931/1932). Anc Mesoam 16:195–211CrossRefGoogle Scholar
  19. Emery KF (2001) The economics of bone artifact production in the ancient Maya lowlands. In: Choyke AM, Bartosiewicz L (eds) In: Crafting bone: skeletal technologies through time and space. Proceedings of the 2nd meeting of the ICAZ worked bone research group, vol 937. Budapest British Archaeological Reports International Series, Oxford, pp 73–84Google Scholar
  20. Emery KF (2005) Animales y rituales en la acropolis de Copan: zoo/arqueologia de dépositos especiales. FAMSI. Accessed 10 Dec 2009
  21. Engstrom TN, Edwards T, Osentoski MF, Myers EM (2007) In: Shafer HB, FitzSimmons NN, Georges A, Rhodin AGH (eds) A compendium of PCR primers for mtDNA, microsatellite, and other nuclear loci for freshwater turtles and tortoisesin defining turtle diversity. In: Proceedings of a workshop on genetics, ethics, and taxonomy of freshwater turtles and tortoises, Chelonian Research Monographs, 4:124–141Google Scholar
  22. Excoffier L, Smouse PE, Quattreo JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  23. Farias I, Orti G, Sampaio I, Schneider H, Meyer A (2001) The cytochrome b gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. J Mol Evol 53:89–103PubMedGoogle Scholar
  24. FitzSimmons NN, Mortitz C, Limpus CJ, Pope L, Prince R (1997) Gene polymorphisms in Australia green turtle populations and male-biased gene flow. Genetics 147:1843–1854PubMedGoogle Scholar
  25. Flores-Villela O (1993) Herpetofauna of Mexico: distribution and endemism. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of Mexico: origins and distributions. Oxford University Press, New York, pp 253–280Google Scholar
  26. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  27. Fujita MK, Engstrom TN, Starkey DE, Shaffer HB (2004) Turtle phylogeny: insights from a novel nuclear intron. Mol Phylogenet Evol 31:1031–1040PubMedCrossRefGoogle Scholar
  28. Gonzalez Soriano E, Dirzo R, Vogt RC (1997) Historia natural de Los Tuxtlas. UNAM, Mexico DFGoogle Scholar
  29. Goudet J, Raymond M, de Meeûs T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940PubMedGoogle Scholar
  30. Guevara-Chumacero LM, López-Wilchis R, Pedroche FF, Juste J, Ibáñez C, Barriga-Sosa IDLA (2010) Molecular phylogeography of Pteronotus davyi (Chiroptera: Mormoopidae). J Mamm 91:220–232. doi: 10.1644/08-MAMM-A-212R3.1 CrossRefGoogle Scholar
  31. Hauswaldt S, Glenn T (2005) Population genetics of the diamondback terrapin (Malaclemysterrapin). Mol Ecol 14:723–732PubMedCrossRefGoogle Scholar
  32. Hobbs RJ, Mooney A (1998) Broadening the extinction debate: population deletions and additions in California and Western Australia. Conserv Biol 12:271–283CrossRefGoogle Scholar
  33. Hodell DA, Anselmetti FS, Ariztegui D, Brenner M, Curtis JH, Gilli A, Grzesk DA, Guilderson TJ, Muller AD, Bush MB, Correa-Metrio A, Escobar J, Kutterolf S (2008) An 85-ka record of climate change in lowland Central America. Quat Sci Rev 27:1152–1165CrossRefGoogle Scholar
  34. Howeth JG, MCGaugh SE, Hendrickson DA (2008) Contrasting demographic and genetic estimates of dispersal in the endangered coahuilan box turtle: a contemporary approach to conservation. Mol Ecol 17:4209–4221PubMedCrossRefGoogle Scholar
  35. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589PubMedGoogle Scholar
  36. Hughes JB, Daily GC, Ehrlich PR (1997) Population diversity: its extent and extinction. Science 278:689–692PubMedCrossRefGoogle Scholar
  37. Hutchison HJ, Bramble DM (1981) Homology of the plastral scales of the Kinosternidae and related turtles. Herpetologica 37:73–85Google Scholar
  38. Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. Mol Evol 32:128–144CrossRefGoogle Scholar
  39. Iverson JB, Mittermeier RA (1980) Dermatemydidae, Dermatemys Gray. Catalogue of American publications of the society for the study of amphibians and reptiles. 237:1–4.
  40. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6: 13. v. 3.16 Accessed 02 Apr 2010
  41. Jenzen KA, Das I (2008) Cultural exploitation of freshwater turtles in Sarawak, Malaysian Borneo. Chelonian Conserv Biol 7:281–284CrossRefGoogle Scholar
  42. Kaska Y (2000) Genetic structure of Mediterranean sea turtle populations. Turk J Zool 24:191–197Google Scholar
  43. Keogh JS (2009) Evolutionary, behavioral and molecular ecology must meet to achieve long-term conservation goals. Mol Ecol 18:3761–3762PubMedCrossRefGoogle Scholar
  44. Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  45. Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:619–620CrossRefGoogle Scholar
  46. Lamb T, Lydeard C, Walker RB, Gibbons WJ (1994) Molecular systematics of map turtles (Graptemys): a comparison of mitochondrial restriction site versus sequence data. Syst Biol 43:543–559CrossRefGoogle Scholar
  47. Lee JC (1980) An ecogeographic analysis of the herpetofauna of the Yucatan Peninsula. Univ Kansas Mus Nat Hist 67:1–48Google Scholar
  48. Lee JC (1996) The amphibians and reptiles of the Yucatan Peninsula. Cornell University Press, IthacaGoogle Scholar
  49. Lenk P, Fritz U, Joger U, Wink M (1999) Mitochondrial phylogeography of European pond turtle, Emys orbicularis (Linneaeus 1758). Mol Ecol 8:1911–1922PubMedCrossRefGoogle Scholar
  50. Leyden BW (1984) Guatemalan forest synthesis after Pleistocene aridity. Proc Natl Acad Sci USA 81:4856–4859PubMedCrossRefGoogle Scholar
  51. Lopez Castro MC, Rocha Olivares A (2005) The panmixia paradigm of eastern pacific olive ridley turtle revised: consequences for their conservation and evolutionary biology. Mol Ecol 14:3325–3334PubMedCrossRefGoogle Scholar
  52. Maldonado JE, Vila C, Wayne RK (2001) Tripartite genetic subdivisions in the ornate shrew (Sorex ornatus). Mol Ecol 10:127–147PubMedCrossRefGoogle Scholar
  53. Moritz C (1994) Defining evolutionary significant units for conservation. Trends Ecol Evol 9:373–375PubMedCrossRefGoogle Scholar
  54. Mulcahy DG, Morrill BH, Mendelson JR (2006) Historical biogeography of lowland species of toads (Bufo) across the Trans-Mexican Neovolcanic belt and the Isthmus of Tehuantepec. J Biogeogr 33:1889–1904CrossRefGoogle Scholar
  55. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  56. Nylander JA (2004) MrModeltest V. 2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  57. O’Day Sharyn, Jones Van, Neer SW, Ervynck A (eds) (2004) Behaviour behind bones: the zooarchaeology of ritual, religion, status, and identity. Oxbow Books, OxfordGoogle Scholar
  58. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  59. Ray DA, Dever JA, Platt SG, Rainwater TR, Finger AG, McMurry ST, Batzer MA, Barr B, Stafford PJ, McKnight J, Densmore LD (2004) Low levels of nucleotide diversity in Crocodylus moreletii and evidence of hybridization with C. acutus. Conserv Genet 5:449–462CrossRefGoogle Scholar
  60. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  61. Reynoso VH (2005) Research on fossil amphibians and reptiles in Mexico, from 1869 to early 2004 (including marine forms but excluding pterosaurs, dinosaurs, and obviously, birds). In: Vega J, Nyborg TG, Perrilliat MC, Montellano-Ballesteros M, Cevallos-Ferriz S, Quiroz-Barroso S (eds) Studies on Mexican paleontology. Springer, The Netherlands, pp 209–231Google Scholar
  62. Rhodin AGJ, Parham JF, van Dijk PP, Iverson JB (2009) Turtles of the world: annotated checklist of taxonomy and synonymy. conservation biology of freshwater turtles and tortoises. Chelonian Res Monogr 5:39–84Google Scholar
  63. Rico Y, Lorenzo C, González-Cózatl FX, Espinoza E (2008) Phylogeography and population structure of the endangered Tehuantepec jackrabbit Lepus flavigularis: implications for conservation. Conserv Genet 9:1467–1477CrossRefGoogle Scholar
  64. Robertson JM, Zamudio KR (2009) Genetic diversification, vicariance and selection in a polytypic frog. J Hered 6:715–731CrossRefGoogle Scholar
  65. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  66. Rozas J, Sánchez-DelBarrio JC, Messenguer X, Rozas R (2003) DNASP, DNA polymorphism analyses by coalescencent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  67. Rozen S, Skaletsky H (1999) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols. Methods in molecular biology, vol 132. Humana Press, Totowa, pp 365–386CrossRefGoogle Scholar
  68. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  69. Savage JM (1966) The origins and history of the Central American herpetofauna. Copeia 4:719–766CrossRefGoogle Scholar
  70. Savage JM (1982) The enigma of the Central American herpetofauna: dispersal or vicariance. Mo Bot Gard 69:464–547CrossRefGoogle Scholar
  71. Soustelle J (2003) Los Olmecas. Fondo de Cult Econ, MéxicoGoogle Scholar
  72. Spinks PQ, Shaffer HB (2005) Range-wide molecular analysis of the western pond turtle (Emys marmorata): cryptic variation, isolation by distance, and their conservation implications. Mol Ecol 14:2047–2064PubMedCrossRefGoogle Scholar
  73. Stanley HF, Casey S, Carnahan JM, Goodman S, Harwood J, Wayne RK (1996) Worldwide patterns of mitochondrial DNA differentiation in the harbor seal (Phoca vitulina). Mol Biol Evol 13:368–382PubMedGoogle Scholar
  74. Starkey DE, Shaffer HB, Burke RL, Forstner MRJ, Iverson JB, Janzen FJ, Rhodin AGI, Ultsch GR (2003) Molecular systematics, phylogeography, and the effects of Pleistocene glaciations in the painted turtle (Chrysemys picta) complex. Evolution 57:119–128PubMedGoogle Scholar
  75. Stuart LC (1957) Herpetofaunal dispersal routes through northern Central America. Copeia 2:89–94CrossRefGoogle Scholar
  76. Stuart LC (1958) A study of the herpetofauna of the Uaxactún-Tikal area of northern El Peten, Guatemala. Contributions from the Laboratory of Vertebrate Biology University of Michigan 75:1–30Google Scholar
  77. Stuart LC (1966) The environment of Central American cold-blooded vertebrate fauna. Copeia 4:684–699CrossRefGoogle Scholar
  78. Stuart BL, Parham JF (2004) Molecular phylogeny of the critically endangered Indochinese box turtle (Cuora galbinifrons). Mol Phylogenet Evol 31:164–177PubMedCrossRefGoogle Scholar
  79. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (and other methods) 4.0 beta. Sinauer, SunderlandGoogle Scholar
  80. Syed GP, Ota H, Buhlmann KA, Forstner MRJ (2007) Genetic considerations in the captive breeding and translocation of freshwater turtles and tortoises for conservation. Chelonian Research Monographs, In: Shaffer HB, FitzSimmons NN, Georges A, Rhodin AGJ (eds). In: Defining turtle diversity. Proceedings of a workshop on genetics, ethics, and taxonomy of freshwater turtles and tortoises, Chelonian Research Monographs, Cambridge MA, 8–12 August 2005Google Scholar
  81. Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143:1457–1465PubMedGoogle Scholar
  82. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  83. Turtle Conservation Fund (2002) A global action plan for conservation of tortoises and freshwater turtles, Strategy and funding prospectus 2002–2007. Conservation International and Chelonian Research Foundation, Washington, DCGoogle Scholar
  84. Vogt RC, Gonzalez-Porter GP, Van Dijk PP (2005) Dermatemys mawii. In: 2006 IUCN red list of threatened species. Accessed 20 Jan 2008
  85. West RC (1964) The natural regions of MiddleAmerica. In: Wauchope R (ed) Handbook of middle American Indians. Natural environment and early cultures, vol 1. University of Texas Press, Austin, p 570Google Scholar
  86. Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST not equal 1/(4Nm + 1). Heredity 82:117–125PubMedCrossRefGoogle Scholar
  87. Ximenez FF (1967) Historia natural del reino de Guatemala, 1st edn. Editorial José de Pineda Ibarra, GuatemalaGoogle Scholar

Copyright information

© US Government 2011

Authors and Affiliations

  • Gracia P. González-Porter
    • 1
    • 2
  • Frank Hailer
    • 1
  • Oscar Flores-Villela
    • 2
  • Rony García-Anleu
    • 3
  • Jesús E. Maldonado
    • 1
    • 4
  1. 1.Center for Conservation and Evolutionary GeneticsSmithsonian Conservation Biology InstituteWashingtonUSA
  2. 2.Museo de Zoología Facultad de CienciasUniversidad Nacional Autónoma de MéxicoMéxico CityMéxico
  3. 3.Wildlife Conservation Society-Guatemala ProgramFloresGuatemala
  4. 4.Department of Vertebrate ZoologyNational Museum of Natural History, Smithsonian InstitutionWashingtonUSA

Personalised recommendations