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Organisms Diversity & Evolution

, Volume 14, Issue 3, pp 279–293 | Cite as

A phylogeny of softshell turtles (Testudines: Trionychidae) with reference to the taxonomic status of the critically endangered, giant softshell turtle, Rafetus swinhoei

  • Minh LeEmail author
  • Ha T. Duong
  • Long D. Dinh
  • Truong Q. Nguyen
  • Peter C. H. Pritchard
  • Timothy McCormack
Original Article

Abstract

Several important aspects of the evolution of the softshell turtle (family Trionychidae) have not been addressed thoroughly in previous studies, including the pattern and timing of diversification of major clades and species boundaries of the critically endangered Shanghai Softshell Turtle, Rafetus swinhoei. To address these issues, we analyzed data from two mitochondrial loci (cytochrome b and ND4) and one nuclear intron (R35) for all species of trionychid turtles, except Pelochelys signifera, and for all known populations of Rafetus swinhoei in Vietnam and one from China. Phylogenetic analyses using three methods (maximum parsimony, maximum likelihood, and Bayesian inference) produce a well resolved and strongly supported phylogeny. The results of our time-calibration and biogeographic optimization analyses show that trionychid dispersals out of Asia took place between 45 and 49 million years ago in the Eocene. Interestingly, the accelerated rates of diversification and dispersal within the family correspond surprisingly well to global warming periods between the mid Paleocene and the early Oligocene and from the end of the Oligocene to the mid Miocene. Our study also indicates that there is no significant genetic divergence among monophyletic populations of Rafetus swinhoei, and that previous taxonomic revision of this species is unwarranted.

Keywords

Trionychidae Rafetus swinhoei Systematics Evolution Africa Asia Europe North America ND4 cytb R35 

Notes

Acknowledgments

The Turtle Conservation Fund generously provided research funding for this project. Field work of T. Q.N. in Vietnam was supported by the Project “The Red Data Book of Vietnam” (Grant No. DTDL.2011-G/23). We are grateful to Nguyen Van Thanh for laboratory assistance and helpful discussions, Ms. Le Thanh Hieu and Vu Dang Dong for support and to Le Sy Vinh and Dang Cao Cuong for computer assistance. Comments from four anonymous reviewers greatly improved the paper.

Supplementary material

13127_2014_169_MOESM1_ESM.docx (574 kb)
ESM 1 (DOCX 574 kb)

References

  1. Arévalo, E., Davis, S. K., & Sites, J. W. (1994). Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Systematic Biology, 43, 387–418.CrossRefGoogle Scholar
  2. Baillie, J. E. M., & Butcher, E. R. (2012). Priceless or Worthless? The World Most Threatened Species. London: Zoological Society of London.Google Scholar
  3. Barley, A. J., Spinks, P. Q., Thomson, R. C., & Shaffer, H. B. (2010). Fourteen nuclear genes provide phylogenetic resolution for difficult nodes in the turtle tree of life. Molecular Phylogenetics and Evolution, 55, 1189–1194.PubMedCrossRefGoogle Scholar
  4. Beard, C. (2002). East of Eden at the Paleocene/Eocene boundary. Science, 295, 2028–2029.PubMedCrossRefGoogle Scholar
  5. Blois, J. L., & Hadly, E. A. (2009). Mammalian response to Cenozoic climate change. Annual Review of Earth and Planetary Sciences, 37, 181–208.CrossRefGoogle Scholar
  6. Bowen, G. J., Clyde, W. C., Koch, P. L., Ting, S., Alroy, J., Tsubamota, T., et al. (2002). Mammalian dispersal at the Paleocene/Eocene boundary. Science, 295, 2062–2065.PubMedCrossRefGoogle Scholar
  7. Brandley, M. C., Schmitz, A., & Reeder, T. W. (2005). Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology, 54, 373–390.PubMedCrossRefGoogle Scholar
  8. Brinkman, D. B. (2003). A review of nonmarine turtles from the Late Cretaceous of Alberta. Canadian Journal of Earth Sciences, 40, 557–571.CrossRefGoogle Scholar
  9. Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.PubMedCrossRefGoogle Scholar
  10. Danilov, I. G. (2005). Die fossilen Schildkröten Europas. In U. Fritz (Ed) Handbuch der Reptilien und Amphibien Europas. Bd. 3, 3B, Schildkröten (Testudines) II, pp. 329–441.Google Scholar
  11. Danilov, I. G., & Vitek, N. S. (2013). Cretaceous trionychids of Asia: an expanded review of their record and biogeography. In D. B. Brinkman, P. A. Holroyd, J. D. Gardner (Eds) Morphology and Evolution of Turtles, pp. 419–438.Google Scholar
  12. de Lapparent de Broin, F. (2000). African chelonians from the Jurassic to the present: phases of development and preliminary catalogue of the fossil record. Palaeontologia Africana, 36(43), 82.Google Scholar
  13. de Lapparent de Broin, F. (2001). The European turtle fauna from the Triassic to the Present. Dumerilia, 4, 155–217.Google Scholar
  14. Drosopoulou, E., Tsiamis, G., Mavropoulou, M., Vittas, S., Katselidis, K. A., Schofield, G., et al. (2012). The complete mitochondrial genome of the loggerhead turtle Caretta caretta (Testudines: Cheloniidae): genome description and phylogenetic considerations. Mitochondrial DNA, 23, 1–12.PubMedCrossRefGoogle Scholar
  15. Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.PubMedCentralPubMedCrossRefGoogle Scholar
  16. Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, 699–710.CrossRefGoogle Scholar
  17. Duellman, W. E. (1999). Patterns of Distribution of Amphibians: A Global Perspective. Baltimore and London: John Hopkins University Press.Google Scholar
  18. Engstrom, T. N., Shaffer, H. B., & Mccord, W. P. (2002). Phylogenetic diversity of endangered and critically endangered southeast Asian softshell turtles (Trionychidae: Chitra). Biological Conservation, 104, 173–179.CrossRefGoogle Scholar
  19. Engstrom, T. N., Shaffer, H. B., & Mccord, W. P. (2004). Multiple data sets, high homoplasy, and the phylogeny of softshell turtles (Testudines: Trionychidae). Systematic Biology, 53, 693–710.PubMedCrossRefGoogle Scholar
  20. Ernst, H. C., & Barbour W. R. (1989). Turtles of the World. Smithsonian Institution PressGoogle Scholar
  21. Farkas, B., Le, M. D., & Nguyen, T. Q. (2011). Rafetus vietnamensis Le, Le, Tran, Phan, Phan, Tran, Pham, Nguyen, Nong, Phan, Dinh, Truong and Ha, 2010—another invalid name for an invalid species of softshell turtle (Reptilia: Testudines: Trionychidae). Russian Journal of Herpetology, 18, 65–72.Google Scholar
  22. Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.CrossRefGoogle Scholar
  23. Fiorillo, A. R. (1999). Non-mammalian microvertebrate remains from the Robison Egghell Site, Cedar Mountain Formation (Lower Cretaceous) Emery County, Utah. In D. D. Gillette (Ed.), Vertebrate Paleontology in Utah (pp. 259–268). Utah Geological Survey, Salt Lake City, UT: Miscellaneous Publication.Google Scholar
  24. Fritz, U., Branch, W. R., Hofmeyr, M. D., Maran, J., Prokop, H., Schleicher, A., Stuckas, H., Vargas-Ramírez, M., Vences, M., & Hundsdörfer, A. K. (2011). Molecular phylogeny of African hinged and helmeted terrapins (Testudines: Pelomedusidae: Pelusios and Pelomedusa). Zoologica Scripta, 40, 115–125.Google Scholar
  25. Fritz, U., Gong, S., Auer, M., Kuchling, G., Schneeweiss, N., & Hundsdörfer, A. K. (2010). The world’s economically most important chelonians represent a diverse species complex (Testudines: Trionychidae: Pelodiscus). Organisms, Diversity & Evolution, 10, 227–242.CrossRefGoogle Scholar
  26. Fujita, M. K., Engstrom, T. N., Starkey, D. E., & Shaffer, H. B. (2004). Turtle phylogeny: Insights from a novel nuclear intron. Molecular Phylogenetics and Evolution, 31, 1031–1040.PubMedCrossRefGoogle Scholar
  27. Gaffney, E. S., & Bartholomai, A. (1979). Fossil trionychids of Australia. Journal of Paleontology, 53, 1354–1360.Google Scholar
  28. Gardner, J. D., Russell, A. P., & Brinkman, D. B. (1995). Systematics and taxonomy of soft- Shelled turtles (family Trionychidae) from the Judith River Group (mid-Campanian) of North America. Canadian Journal of Earth Sciences, 32, 631–643.CrossRefGoogle Scholar
  29. Gidis, M., Spinks, P. Q., Çevik, E., Kaska, Y., & Shaffer, H. B. (2011). Shallow genetic divergence indicates a Congo-Nile riverine connection for the softshell turtle Trionyx triunguis. Conservation Genetics, 12, 589–594.CrossRefGoogle Scholar
  30. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium, 41, 95–98.Google Scholar
  31. Head, J. J., Aguilera, O. A., & Sánchez-Villagra, M. R. (2006). Past colonization of South America by trionychid turtles: Fossil evidence from Neogene of Margarita Island Venezuela. Journal of Herpetology, 40, 378–381.CrossRefGoogle Scholar
  32. Hillis, D. M., & Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182–192.CrossRefGoogle Scholar
  33. Hirayama, R., Brinkman, D. B., & Danilov, I. G. (2000). Distribution and biogeography of non- marine Cretaceous turtles. Russian Journal of Herpetology, 7, 181–198.Google Scholar
  34. Iverson, J. B. (1992). A revised checklist with distribution maps of the turtles of the world. Richmond, Indiana: Privately published.Google Scholar
  35. Joyce, W. G., & Lyson, T. R. (2010). A neglected lineage of North American turtles fills a major gap in the fossil record. Palaeontology, 53, 241–248.CrossRefGoogle Scholar
  36. Kasparek, M. (2001). Priorities for the conservation of the Nile softshelled turtle, Trionyx triunguis in the Mediterranean. Testudo, 5, 49–59.Google Scholar
  37. Krenz, J. G., Naylor, G. J. P., Shaffer, H. B., & Janzen, F. J. (2005). Molecular phylogenetics and evolution of turtles. Molecular Phylogenetics and Evolution, 37, 178–191.PubMedCrossRefGoogle Scholar
  38. Kuchling, G. (2012). Field surveys for wild Rafetus. Available at www.turtlesurvival.org/blog/1-blog/167-field-surveys-for-wild-rafetus. Accessed on July 8, 2013
  39. Le, M., & McCord, W. P. (2008). Phylogenetic relationships and biogeographical history of the genus Rhinoclemmys Fitzinger, 1835 and the monophyly of the turtle family Geoemydidae (Testudines: Testudinoidea). Zoological Journal of Linnean Society, 153, 751–767.CrossRefGoogle Scholar
  40. Le, M., & Pritchard, C. H. P. (2009). Genetic variability of the critically endangered softshell turtle, Rafetus swinhoei: A preliminary report. Proceedings of the First Vietnamese National Symposium on Reptiles and Amphibians, pp. 84–92.Google Scholar
  41. Le, M., McCord, W. P., & Iverson, J. B. (2007). On the paraphyly of the genus Kachuga (Testudines: Geoemydidae). Molecular Phylogenetics and Evolution, 45, 398–404.PubMedCrossRefGoogle Scholar
  42. Le, T. B., Le, Q. H., Tran, M. L., Phan, T. H., Phan, M. T., Tran, T. T. H., et al. (2010). Comparative morphological and DNA analysis of specimens of giant freshwater soft-shelled turtle in Vietnam related to Hoan Kiem Lake. Vietnam Journal of Biotechnology, 8, 949–954.Google Scholar
  43. Liebing, N., Praschag, P., Gosh, R., Vasudevan, K., Rashid, S. M. A., Rao, D. Q., et al. (2012). Molecular phylogeny of the softshell turtle genus Nilssonia revisited, with first records of N. formosa for China and wild-living N. nigricans for Bangladesh. Vertebrate Zoology, 62, 261–272.Google Scholar
  44. McGaugh, S. E., Eckerman, C. M., & Janzen, F. J. (2008). Molecular phylogeography of Apalone spinifera (Reptilia, Trionychidae). Zoologica Scripta, 37, 289–304.CrossRefGoogle Scholar
  45. McKenna, M. C. (1983). Cenozoic paleogeography of North Atlantic land bridges. In M. H. P. Bott, S. Saxov, M. Talwani, & J. Thiede (Eds.), Structure and Development of the Greenland-Scotland Bridge: New Concepts and Methods (pp. 351–395). New York: Plenum.CrossRefGoogle Scholar
  46. Meylan, A. P. (1987). The phylogenetic relationships of soft-shelled turtles (family Trionychidae). Bulletin of the American Museum of Natural History, 186, 1–101.Google Scholar
  47. Moreau, C. S., Bell, C. D., Vila, R., Archibald, S. B., & Pierce, N. E. (2006). Phylogeny of the ants: diversification in the age of angiosperms. Science, 312, 101–104.PubMedCrossRefGoogle Scholar
  48. Naro-Maciel, E., Le, M., Fitzsimmons, N. N., & Amato, G. (2008). Evolutionary relationships of marine turtles: a molecular phylogeny based on nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution, 49, 659–662.PubMedCrossRefGoogle Scholar
  49. Nessov, L. A. (1995). On some Mesozoic turtles of the Fergana Depression (Kyrgyzstan) and Dzhugar Alatau Ridge (Kazakhstan). Russian Journal of Herpetology, 2, 134–141.Google Scholar
  50. Nylander, J. A. A., Ronquist, F., Huelsenbeck, J. P., & Nieves-Aldrey, J. L. (2004). Bayesian phylogenetic analysis of combined data. Systematic Biology, 53, 47–67.PubMedCrossRefGoogle Scholar
  51. Palumbi, S. R. (1996). Nucleic acids II: The polymerase chain reaction. In D. M. Hillis, C. Moritz, & B. K. Mable (Eds.), Molecular systematic (2nd ed., pp. 205–247). Sunderland, MA: Sinauer Associates.Google Scholar
  52. Posada, D., & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.PubMedCrossRefGoogle Scholar
  53. Praschag, P., Hundsdörfer, A. K., Reza, A. H. M. A., & Fritz, U. (2007). Genetic evidence for wild- living Aspideretes nigricans and molecular phylogeny of South Asian softshell turtles (Reptilia: Trionychidae: Aspideretes, Nilssonia). Zoologica Scripta, 36, 301–310.CrossRefGoogle Scholar
  54. Praschag, P., Stuckas, H., Päckert, M., Maran, J., & Fritz, U. (2011). Mitochondrial DNA sequences suggest a revised taxonomy of Asian flap shell turtles (Lissemys Smith, 1931) and the validity of previously unrecognized taxa (Testudines: Trionychidae). Vertebrate Zoology, 61, 147–160.Google Scholar
  55. Pritchard, P. C. H. (2001). Observations on body size, sympatry, and niche divergence in softshell turtles (Trionychidae). Chelonian Conservation and Biology, 4, 5–27.Google Scholar
  56. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.PubMedCentralPubMedCrossRefGoogle Scholar
  57. Sanmartin, I., Enghoff, H., & Ronquist, F. (2001). Patterns of animal dispersal, vicariance and diversification in the Holarctic. Biological Journal of the Linnean Society, 73, 345–390.CrossRefGoogle Scholar
  58. Scheyer, M. T., Mörs, T., & Einarsson, E. (2012). First record of soft-shelled turtles (Cryptodira, Trionychidae) from the late Cretaceous of Europe. Journal of Vertebrate Paleontology, 32, 1027–1032.CrossRefGoogle Scholar
  59. Smith, T., Rose, K. D., & Gingerich, P. D. (2006). Rapid Asia-Europe-North America geographic dispersal of earliest Eocene primate Teilhardina during the Paleocene-Eocene thermal maximum. Proceedings of the National Academy of Sciences, 103, 11223–11227.CrossRefGoogle Scholar
  60. Stadler, T. (2011). Stimulating trees on a fixed number of extant species. Systematic Biology, 60, 676–684.PubMedCrossRefGoogle Scholar
  61. Stuckas, H., & Fritz, U. (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). Journal of Zoological Systematics and Evolutionary Research, 49, 335–339.CrossRefGoogle Scholar
  62. Swofford, D. L. (2001). PAUP* Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA: Sinauer Associates.Google Scholar
  63. Templeton, A. R., Crandall, K. A., & Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619–633.PubMedCentralPubMedGoogle Scholar
  64. Van Dijk, P. P., Iverson, J. B., Shaffer, H. B., Bour, R., & Rhodin, A. G. J. (2012). Turtles of the world, 2012 update: annotated checklist of taxonomy, synonymy, distribution, and conservation status. Chelonian Research Monographs, 5, 243–328.Google Scholar
  65. Vieites, D. R., Min, M.-S., & Wake, D. B. (2007). Rapid diversification and dispersal during periods of global warming by plethodontid salamanders. Proceedings of the National Academy of Sciences, 104, 19903–19907.CrossRefGoogle Scholar
  66. Vitek, N. S., & Danilov, I. G. (2010). New material and a reassessment of soft-shelled turtles (Trionychidae) from the late Cretaceous of middle Asia and Kazakhstan. Journal of Vertebrate Paleontology, 30, 383–393.CrossRefGoogle Scholar
  67. Wang, J., & Shi, H. T. (2011). The change of historical distribution of Rafetus swinhoei. Acta Zootaxonomica Sinica, 36, 919–924.Google Scholar
  68. Weisrock, D. W., & Janzen, F. J. (2000). Comparative molecular phylogeography of North American softshell turtles (Apalone): implications for regional and wide-scale historical evolutionary forces. Molecular Phylogenetics and Evolution, 14, 152–164.PubMedCrossRefGoogle Scholar
  69. Wood, R. C., & Patterson, B. (1973). A fossil trionychid turtle from South America. Breviora, 405(1), 10.Google Scholar
  70. Yang, P., Tang, Y., Ding, L., Guo, X., & Wang, Y. (2011). Validity of Pelodiscus parviformis (Testudines: Trionychidae) inferred from molecular and morphological analyses. Asian Herpetological Research, 2, 21–29.CrossRefGoogle Scholar
  71. Yu, Y., Harris, A.J., He, & X.J. (2011). RASP (reconstruct ancestral state in phylogenies). http://mnh.scu.edu.cn/soft/blog/RASP.
  72. Zachos, J., Pagani, M., Sloan, L., Thomas, E., & Billups, K. (2001). Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292, 686–693.PubMedCrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2014

Authors and Affiliations

  • Minh Le
    • 1
    • 2
    • 3
    Email author
  • Ha T. Duong
    • 4
  • Long D. Dinh
    • 4
    • 9
  • Truong Q. Nguyen
    • 5
    • 6
  • Peter C. H. Pritchard
    • 7
  • Timothy McCormack
    • 8
  1. 1.Department of Environmental Ecology, Faculty of Environmental ScienceHanoi University of Science, VNUHanoiVietnam
  2. 2.Centre for Natural Resources and Environmental StudiesVNUHanoiVietnam
  3. 3.Department of Herpetology, Division of Vertebrate ZoologyAmerican Museum of Natural HistoryNew YorkUSA
  4. 4.Department of Genetics, Faculty of BiologyHanoi University of Science, VNUHanoiVietnam
  5. 5.Institute of Ecology and Biological ResourcesVietnam Academy of Science and TechnologyHanoiVietnam
  6. 6.Department of Terrestrial Ecology, Cologne BiocenterUniversity of CologneCologneGermany
  7. 7.Chelonian Research InstituteOviedoUSA
  8. 8.Asian Turtle ProgramCleveland Metroparks ZooHanoiVietnam
  9. 9.Department of Fundamental SciencesVNU-School of Medicine and PharmacyHanoiVietnam

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