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Problems of the Ancestry of Turtles

  • Robert L. CarrollEmail author
Part of the Vertebrate Paleobiology and Paleoanthropology book series (VERT)

Abstract

The unquestioned unity of the Chelonia provides a necessary basis for establishing their interrelationships and determining the evolutionary history within the group. On the other hand, the host of uniquely derived features of the oldest known turtles make it extremely difficult to establish their ancestry among more primitive amniotes. This is illustrated by the great diversity of taxa that continue to be proposed as putative sister-taxa of turtles without general acceptance of any. Nearly every major clade of early amniotes from the late Paleozoic and early Mesozoic has been proposed as a possible sister-taxon of turtles, from synapsids to anapsids and diapsids, including pelycosaurs, captorhinomorphs, procolophonids, pareiasaurs, aquatic placodonts and crocodiles, but none possess derived characters that could be synapomorphic with the unique skeletal structure and patterns of development of the chelonian skull, carapace or plastron, which had reached an essentially modern configuration by the Late Triassic. Numerous molecular biologists have attempted to establish the closest sister-group of turtles through analyses of a host of living species, but there is no way for them to preclude turtles from having evolved from one or another of the Paleozoic or early Mesozoic clades that have become extinct without leaving any other living descendants. On the other hand, recent studies of the genetic and molecular aspects of the development of the carapace and plastron imply unique patterns of evolutionary change that cannot be recognized in any of the other amniote lineages, living or dead. This, together with the retention of a skull without temporal fenestration implies a very early divergence from a lineage that probably retained an anapsid skull configuration. This problem may be resolved by more detailed study of the enigmatic genus Eunotosaurus, from the Late Permian of South Africa.

Keywords

Captorhinomorphs Eunotosaurus Pareiasaurs Procolophonids Turtle origins 

Notes

Acknowledgments

I would like to thank Don Brinkman for bringing together the many colleagues of Gene Gaffney for this symposium in his honor, and for arranging the publication of the many resulting lectures and discussions. I would also like to recognize the assistance of Mary-Ann Lacey for assembling and labeling the many drawing that help in understanding the nature of the putative sister taxa of turtles, and Trond Sigurdsen for their final integration in this paper. It should also be noted that understanding of the origin and evolution of turtles could not have reached the level that has been achieved to date if it were not for the continuing research of many scientists studying molecular and genetic aspects of the development of modern turtles. The financial support for assembling the data required for this paper and travel to scientific meetings where it was discussed was provided by the National Science Foundation of Canada.

References

  1. Ax, P. (1984). Das phylogenetische system. Stuttgart: Fischer.Google Scholar
  2. Burke, A. C. (1989). Development of the turtle carapace: Implications for the evolution of a novel bauplan. Journal of Morphology, 1999, 363–378.CrossRefGoogle Scholar
  3. Cao, Y., Sorenson, M. D., Kumazawa, Y., Mindell, D. P., & Hasegawa, M. (2000). Phylogenetic position of turtles among amniotes: Evidence from mitochondrial and nuclear genes. Gene, 259, 139–148.CrossRefGoogle Scholar
  4. Carroll, R. L. (1969). A Middle Pennsylvanian captorhinomorph, and the interrelationships of primitive reptiles. Journal of Paleontology, 43, 151–170.Google Scholar
  5. Carroll, R. L. (1988). Vertebrate paleontology and evolution. New York: W. H. Freeman & Co.Google Scholar
  6. Cebra-Thomas, J., Tan, F., Sistla, S., Estes, E., Bender, G., Kim, C., et al. (2005). How the turtle forms its shell: A paracrine hypothesis of carapace formation. Journal of Experimental Zoology B, 304, 558–569.CrossRefGoogle Scholar
  7. Cebra-Thomas, J. A., Betters, E., Yin, M., Plafkin, C., McDow, K., & Gilbert, S. F. (2007). Evidence that a late-emerging population of trunk neural crest cells forms the plastron bones in the turtle Trachemys scripta. Evolution & Development, 9, 267–277.CrossRefGoogle Scholar
  8. Clark, K., Bender, G., Murray, B. P., Panfilio, K., Cook, S., Davis, R., et al. (2001). Evidence for the neural crest origin of turtle plastron bones. Genesis, 31, 111–117.CrossRefGoogle Scholar
  9. Cox, C. B. (1969). The problematic Permian reptile Eunotosaurus. Bulletin of the British Museum (Geology), 18, 165–196.Google Scholar
  10. Currie, P. J. (1977). A new haptodontine sphenacodont (Reptilia; Pelycosauria) from the Upper Pennsylvanian of North America. Journal of Paleontology, 51, 927–942.Google Scholar
  11. De Beer, G. S. (1937). The development of the vertebrate skull. Oxford: Clarendon Press.Google Scholar
  12. deBraga, M., & Rieppel, O. (1997). Reptile phylogeny and the interrelationships of turtles. Zoological Journal of the Linnean Society, 120, 281–354.CrossRefGoogle Scholar
  13. Gaffney, E. S. (1980). Phylogenetic relationships of the major groups of amniotes other than turtles. In A. L. Panchen (Ed.), The terrestrial environment and the origin of land vertebrates (pp. 593–610). London: Academic Press.Google Scholar
  14. Gaffney, E. S. (1990). The comparative osteology of the Triassic turtle Proganochelys. Bulletin of the American Museum of Natural History, 194, 1–263.Google Scholar
  15. Gaffney, E. S., & Jenkins, F. (2010). The cranial morphology of Kayentachelys, an Early Jurassic cryptodire, and the early history of turtles. Acta Zoologica (Stockholm), 91, 335–368.Google Scholar
  16. Gaffney, E. S., & McKenna, M. C. (1979). A Late Permian captorhinid from Rhodesia. American Museum Novitates, 2688, 1–15.Google Scholar
  17. Gaffney, E. S., & Meeker, L. J. (1983). Skull morphology of the oldest turtles: A preliminary description of Proganochelys quenstedti. Journal of Vertebrate Paleontology, 3, 25–28.CrossRefGoogle Scholar
  18. Gaffney, E. S., & Meylan, P. A. (1988). A phylogeny of turtles. In M. J. Benton (Ed.), The phylogeny and classification of tetrapods (pp. 147–219). Oxford: Clarendon Press.Google Scholar
  19. Gardiner, B. G. (1982). Tetrapod classification. Zoological Journal of the Linnean Society, 74, 207–232.CrossRefGoogle Scholar
  20. Gardiner, B. G. (1993). Haematothermia: Warm-blooded amniotes. Cladistics, 9, 369–395.CrossRefGoogle Scholar
  21. Gilbert, S., Loredo, G., Brukman, A., & Burke, A. (2001). Morphogenesis of the turtle shell: The development of a novel structure in tetrapod evolution. Evolution & Development, 3, 47–58.CrossRefGoogle Scholar
  22. Gilbert, S. F., Cebra-Thomas, J. A., & Tan, F. (2004). Working hypothesis for the origin of the turtle shell. Journal of Morphology, 260, 294.Google Scholar
  23. Goette, A. (1899). Über die Entwicklung des knöchernen Rückenschildes (Carapax) der Schildkröten. Zeitschrift für wissenschaftliche Zoologie, 66, 407–434.Google Scholar
  24. Gradstein, F., Ogg, J., & Smith, A. (2004). A geologic time scale 2004. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  25. Hedges, S. B., & Poling, L. (1999). A molecular phylogeny of reptiles. Science, 283, 998–9001.CrossRefGoogle Scholar
  26. Hofsten, N. (1941). On the phylogeny of the Reptilia. Zoologisca Bidrag Fran Uppsala, 20, 501–521.Google Scholar
  27. Hugall, A. F., Foster, R., & Lee, M. S. Y. (2007). Calibration choice, rate smoothing and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. Systematic Biology, 56, 543–563.CrossRefGoogle Scholar
  28. Iwabe, N., Hara, Y., Kumazawa, Y., Shibamoto, K., Saito, Y., Miyata, T., & Katoh, K. (2005). Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. Molecular Biology and Evolution, 22, 810–813.CrossRefGoogle Scholar
  29. Keyser, A. W., & Gow, C. E. (1981). First complete skull of the Permian reptile Eunotosaurus africanus Seeley. South African Journal of Science, 77, 417–420.Google Scholar
  30. Krenz, J. G., Naylor, J. P., Shaffer, H. B., & Jazen, F. J. (2005). Molecular phylogenetics and evolution of turtles. Molecular Phylogenetics and Evolution, 37, 178–191.CrossRefGoogle Scholar
  31. Kumazawa, Y. (2007). Mitochondrial genomes from the major lizard families suggest their phylogenetic relationships and ancient radiations. Gene, 388, 19–26.CrossRefGoogle Scholar
  32. Kuraku, S., Usuda, R., & Kuratani, S. (2005). Comprehensive survey of carapacial ridge-specific genes in turtles implies co-option of some regulatory genes in carapace evolution. Evolution & Development, 7, 3–17.CrossRefGoogle Scholar
  33. Laurin, M., & Reisz, R. R. (1995). A reevaluation of early amniote phylogeny. Biological Journal of the Linnean Society, 101, 59–95.CrossRefGoogle Scholar
  34. Lee, M. S. Y. (1993). The origin of the turtle body plan: Bridging a famous morphological gap. Science, 261, 1716–1720.CrossRefGoogle Scholar
  35. Lee, M. S. Y. (1994). The turtle’s long-lost relatives. Natural History, 103, 63–65.Google Scholar
  36. Lee, M. S. Y. (1995). Historical Burden in systematics and the interrelationships of ‘parareptiles’. Biological Reviews, 70, 459–547.CrossRefGoogle Scholar
  37. Lee, M. S. Y. (1996). Correlated progression and the origin of turtles. Nature, 379, 812–815.CrossRefGoogle Scholar
  38. Lee, M. S. Y. (1997). Pareiasaur phylogeny and the origin of turtles. Zoological Journal of the Linnean Society, 120, 197–280.CrossRefGoogle Scholar
  39. Lee, M. S. Y. (2001). Molecules, morphology, and the monophyly of diapsid reptiles. Contributions to Zoology, 70, 1–19.Google Scholar
  40. Lee, M. S. Y., Gow, C. E., & Kitching, J. W. (1997). Anatomy and relationships of the pareiasaur Pareiasuchus nasicornis from the Upper Permian of Zambia. Palaeontology, 40, 307–335.Google Scholar
  41. Li, C., Wu, X.-C., Rieppel, O., & Wang, L.-T. (2008). An ancestral turtle from the Late Triassic of southwestern China. Science, 456, 497–501.Google Scholar
  42. Løvtrup, S. (1977). The Phylogeny of Vertebrates. London: John Wiley.Google Scholar
  43. Løvtrup, S. (1985). On the classification of the taxon Tetrapoda. Systematic Zoology, 34, 463–470.CrossRefGoogle Scholar
  44. Mannen, H., & Steven, S. L. (1999). Molecular evidence for a clade of turtles. Molecular Phylognetics and Evolution, 13, 144–148.CrossRefGoogle Scholar
  45. Moustakas, J. E. (2008). Development of the carapacial ridge: Implications for the evolution of genetic networks in turtle shell development. Evolution & Development, 10, 29–36.CrossRefGoogle Scholar
  46. Olson, E. C. (1947). The family Diadectidae and its bearing on the classification of reptiles. Fieldiana Geology, 11, 2–53.Google Scholar
  47. Reisz, R. (1972). Pelycosaurian reptiles from the Middle Pennsylvanian of North America. Bulletin of the Harvard University Press, 144, 27–61.Google Scholar
  48. Reisz, R. (1977). Petrolacosaurus, the oldest known diapsid reptile. Science, 196, 1091–1093.CrossRefGoogle Scholar
  49. Reisz, R. (1981). A diapsid reptile from the Pennsylvanian of Kansas. Special Publication of the Museum of Natural History, University of Kansas, 7, 1–74.Google Scholar
  50. Reisz, R., & Laurin, M. (1991). Owenetta and the origin of turtles. Nature, 349, 324–326.CrossRefGoogle Scholar
  51. Remane, A. (1959). Die Geschichte der Tiere. In G. Heberer (Ed.), Die evolution der organismen (2nd ed., Vol. 1, pp. 340–422). Stuttgart: Gustav Fischer.Google Scholar
  52. Rieppel, O. (2001). Turtles as hopeful monsters. BioEssays, 23, 987–991.CrossRefGoogle Scholar
  53. Rieppel, O. (2008). The relationships of turtles within amniotes. In J. Wyneken, M. H. Godfrey, & V. Bels (Eds.), Biology of turtles (pp. 345–353). Boco Raton: CRC Press.Google Scholar
  54. Rieppel, O., & Reisz, R. R. (1999). The origin and early evolution of turtles. Annual Reviews of Ecology and Systematics, 30, 1–22.CrossRefGoogle Scholar
  55. Romer, A. S., & Price, L. I. (1940). Review of the Pelycosauria. Geological Society of America Special Paper, 28, 1–538.Google Scholar
  56. Scheyer, T., Brüllmann, T., & Sanchez-Villagra, M. (2008). The ontogeny of the shell in side-necked turtles, with emphasis on the homologies of costal and neural bones. Journal of Morphology, 269, 1008–1021.CrossRefGoogle Scholar
  57. Seeley, H. (1892). On a new reptile from Welte Vreden (Beaufort West) Eunotosaurus africanus (Seeley). Quarterly Journal of the Geological Society London, 48, 583–585.CrossRefGoogle Scholar
  58. Vickaryous, M., & Hall, B. (2008). Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms. Journal of Morphology, 269, 398–422.CrossRefGoogle Scholar
  59. Watson, D. M. S. (1914). Eunotosaurus africanus Seeley, and the ancestry of the Chelonia. Proceedings Zoological Society of London, 1914, 1011–1020.Google Scholar
  60. Werneburg, I., & Sanchez-Villagra, M. R. (2009). Timing of organogenesis support basal position of turtles in the amniote tree of life. BMC Evolutionary Biology, 9, 82. doi: 10.1186/1471-2148-9-82.CrossRefGoogle Scholar
  61. Yntema, C. (1970). Extirpation experiments on the embryonic rudiments of the carapace of Chelydra serpentina. Journal of Morphology, 132, 235–244.CrossRefGoogle Scholar
  62. Zardoya, R., & Meyer, A. (1998). Complete mitochondrial genome suggests diapsid affinities of turtles. Proceedings of the National Academy of Science, 95, 14226–14231.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Redpath MuseumMcGill UniversityMontrealCanada

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