Skip to main content

Advertisement

Log in

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

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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.

    Article  Google Scholar 

  • Baillie, J. E. M., & Butcher, E. R. (2012). Priceless or Worthless? The World Most Threatened Species. London: Zoological Society of London.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Beard, C. (2002). East of Eden at the Paleocene/Eocene boundary. Science, 295, 2028–2029.

    Article  CAS  PubMed  Google Scholar 

  • Blois, J. L., & Hadly, E. A. (2009). Mammalian response to Cenozoic climate change. Annual Review of Earth and Planetary Sciences, 37, 181–208.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Brinkman, D. B. (2003). A review of nonmarine turtles from the Late Cretaceous of Alberta. Canadian Journal of Earth Sciences, 40, 557–571.

    Article  Google Scholar 

  • Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1660.

    Article  CAS  PubMed  Google Scholar 

  • 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.

  • 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.

  • 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 

  • de Lapparent de Broin, F. (2001). The European turtle fauna from the Triassic to the Present. Dumerilia, 4, 155–217.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.

    Article  PubMed Central  PubMed  Google Scholar 

  • Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology, 4, 699–710.

    Article  CAS  Google Scholar 

  • Duellman, W. E. (1999). Patterns of Distribution of Amphibians: A Global Perspective. Baltimore and London: John Hopkins University Press.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Ernst, H. C., & Barbour W. R. (1989). Turtles of the World. Smithsonian Institution Press

  • 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 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.

    Article  Google Scholar 

  • 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 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Gaffney, E. S., & Bartholomai, A. (1979). Fossil trionychids of Australia. Journal of Paleontology, 53, 1354–1360.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Iverson, J. B. (1992). A revised checklist with distribution maps of the turtles of the world. Richmond, Indiana: Privately published.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kasparek, M. (2001). Priorities for the conservation of the Nile softshelled turtle, Trionyx triunguis in the Mediterranean. Testudo, 5, 49–59.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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 

  • McGaugh, S. E., Eckerman, C. M., & Janzen, F. J. (2008). Molecular phylogeography of Apalone spinifera (Reptilia, Trionychidae). Zoologica Scripta, 37, 289–304.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Posada, D., & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Stadler, T. (2011). Stimulating trees on a fixed number of extant species. Systematic Biology, 60, 676–684.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Swofford, D. L. (2001). PAUP* Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wang, J., & Shi, H. T. (2011). The change of historical distribution of Rafetus swinhoei. Acta Zootaxonomica Sinica, 36, 919–924.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Wood, R. C., & Patterson, B. (1973). A fossil trionychid turtle from South America. Breviora, 405(1), 10.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Yu, Y., Harris, A.J., He, & X.J. (2011). RASP (reconstruct ancestral state in phylogenies). http://mnh.scu.edu.cn/soft/blog/RASP.

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Minh Le.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 574 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le, M., Duong, H.T., Dinh, L.D. et al. A phylogeny of softshell turtles (Testudines: Trionychidae) with reference to the taxonomic status of the critically endangered, giant softshell turtle, Rafetus swinhoei . Org Divers Evol 14, 279–293 (2014). https://doi.org/10.1007/s13127-014-0169-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-014-0169-3

Keywords

Navigation