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Three Ways to Tackle the Turtle: Integrating Fossils, Comparative Embryology, and Microanatomy

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Morphology and Evolution of Turtles

Abstract

Herein we review a series of case studies covering the evolution and phylogenesis of turtles, and the ontogenetic development of one of the most peculiar body plans within the Craniota. Comparative analyses of skeletal development, ontogenetic timing, and bone microstructure in both extant and extinct taxa are used to document patterns and make inferences about the origin of turtles, turtle ingroup relationships, and the evolution of turtle ontogenetic development. The need for a balanced sampling of both cryptodiran and pleurodiran turtle species for future comparative studies is highlighted.

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References

  • Burke, A. C. (2009). Turtles…. again. Evolution & Development, 11, 622–624.

    Article  Google Scholar 

  • Carroll, R. L. (2012). Problems of the ancestry of turtles. In D. B. Brinkman, P. A. Holroyd & J. D. Gardner (Eds.), Morphology and evolution of turtles. Dordrecht: Springer.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • deBraga, M., & Rieppel, O. (1997). Reptile phylogeny and the interrelationships of turtles. Zoological Journal of the Linnean Society, 120, 281–354.

    Article  Google Scholar 

  • Delfino, M., Scheyer, T. M., Fritz, U., & Sánchez-Villagra, M. R. (2010). An integrative approach to examining a homology question: Shell structures in soft-shelled turtles. Biological Journal of the Linnean Society, 99, 462–476.

    Article  Google Scholar 

  • Fabrezi, M., Manzano, A., Abdala, V., & Zaher, H. (2009). Developmental basis of limb homology in pleurodiran turtles, and the identity of the hooked element in the chelonian tarsus. Zoological Journal of the Linnean Society, 155, 845–866.

    Article  Google Scholar 

  • Gaffney, E. S., & Meylan, P. A. (1988). A phylogeny of turtles. In M. J. Benton (Ed.), The Phylogeny and Classification of the Tetrapods (Vol. 1, pp. 157–219). Amphibians, Reptiles, Birds. Oxford: Clarendon Press.

    Google Scholar 

  • Gauthier, J., Kluge, A. G., & Rowe, T. (1988). Amniote phylogeny and the importance of fossils. Cladistics, 4, 105–209.

    Article  Google Scholar 

  • Germain, D., & Laurin, M. (2009). Evolution of ossification sequences in salamanders and urodele origins assessed through event-pairing and new methods. Evolution & Development, 11, 170–190.

    Article  Google Scholar 

  • Gilbert, S. F., Loredo, G. A., Brukman, A., & Burke, A. C. (2001). Morphogenesis of the turtle shell: The development of a novel structure in tetrapod evolution. Evolution & Development, 3, 47–58.

    Article  Google Scholar 

  • Gilbert, S. F., Bender, G., Betters, E., Yin, M., & Cebra-Thomas, J. A. (2007). The contribution of neural crest cells to the nuchal bone and plastron of the turtle shell. Integrative and Comparative Biology, 47, 401–408.

    Article  Google Scholar 

  • Hall, B. K. (2005). Bones and cartilage. Developmental and Evolutionary Skeletal Biology. Amsterdam: Elsevier Academic Press.

    Google Scholar 

  • Head, J. J., Hutchison, J. H., & Evans, D. C. (2009). The phylogenetic interrelationships and antiquity of plastomenid turtles. Gaffney Turtle Symposium (October 17–18, 2009, Royal Tyrrell Museum, Drumheller, Canada). Abstract Volume, 71.

    Google Scholar 

  • Herrel, A., Van Damme, J., & Aerts, P. (2008). Cervical anatomy and function in turtles. In J. Wyneken, M. H. Godfrey & V. Bels (Eds.), Biology of Turtles (pp. 163–185). Boca Raton: CRC Press.

    Google Scholar 

  • Hill, R. V. (2005). Integration of morphological data sets for phylogenetic analysis of Amniota: The importance of integumentary characters and increased taxonomic sampling. Systematic Biology, 54, 530–547.

    Article  Google Scholar 

  • Iwabe, N., Hara, Y., Kumazawa, Y., Shibamoto, K., Saito, Y., Miyata, T., et al. (2004). Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA–coded proteins. Molecular Biology and Evolution, 22, 810–813.

    Article  Google Scholar 

  • Jeffery, J. E., Bininda-Emonds, O. R. P., Coates, M. I., & Richardson, M. K. (2005). A new technique for identifying sequence heterochrony. Systematic Biology, 54, 230–240.

    Article  Google Scholar 

  • Joyce, W. G., & Gauthier, J. A. (2004). Palaeoecology of Triassic stem turtles sheds new light on turtle origins. Proceedings of the Royal Society of London, B, 271, 1–5.

    Article  Google Scholar 

  • Joyce, W.G., & Karl, H.-V. (2006). The world’s oldest fossil turtle: Fact versus fiction. Fossil Turtle Research, Vol. 1, Russian Journal of Herpetology, 13(Suppl. 1), 104–111.

    Google Scholar 

  • Joyce, W. G., & Lyson, T. R. (2010). A neglected lineage of North America turtles fills a major gap in the fossil record. Palaeontology, 53, 241–248.

    Article  Google Scholar 

  • Joyce, W. G., Lucas, S. G., Scheyer, T. M., Heckert, A. B., & Hunt, A. P. (2009). A thin-shelled reptile from the Late Triassic of North America and the origin of the turtle shell. Proceedings of the Royal Society of London, B, 276, 507–513.

    Article  Google Scholar 

  • Kuratani, S., Kuraku, S., & Nagashima, H. (2011). Evolutionary developmental perspective for the origin of turtles: The folding theory for the shell based on the developmental nature of the carapacial ridge. Evolution & Development, 13, 1–14.

    Article  Google Scholar 

  • Laurin, M., & Reisz, R. R. (1995). A reevaluation of early amniote phylogeny. Zoological Journal of the Linnean Society, 113, 165–223.

    Article  Google Scholar 

  • Lee, M. S. Y. (1997a). Pareiasaur phylogeny and the origin of turtles. Zoological Journal of the Linnean Society, 120, 197–280.

    Article  Google Scholar 

  • Lee, M. S. Y. (1997b). Reptile relationships turn turtle. Nature, 389, 245–246.

    Article  Google Scholar 

  • Lee, M. S. Y., Reeder, T. W., Slowinski, J. B., & Lawson, R. (2004). Resolving reptile relationships. Molecular and morphological markers. In J. Cracraft & M. J. Donoghue (Eds.), Assembling the Tree of Life (pp. 451–467). Oxford: Oxford University Press.

    Google Scholar 

  • Li, C., Wu, X.-C., Rieppel, O., Wang, L.-T., & Zhao, L.-J. (2008). An ancestral turtle from the Late Triassic of southwestern China. Nature, 456, 497–501.

    Article  Google Scholar 

  • Lyson, T., & Gilbert, S. F. (2009). Turtles all the way down: Loggerheads at the root of the chelonian tree. Evolution & Development, 11, 133–135.

    Article  Google Scholar 

  • Lyson, T. R., Bever, G. S., Bhullar, B.-A. S., Joyce, W. G., & Gauthier, J. A. (2010). Transitional fossils and the origin of turtles. Biology Letters, 6, 830–833.

    Article  Google Scholar 

  • Maxwell, E. E., & Harrison, L. B. (2009). Methods for the analysis of developmental sequence data. Evolution & Development, 11, 109–119.

    Article  Google Scholar 

  • Müller, J. (2003). Early loss and multiple return of the lower temporal arcade in diapsid reptiles. Naturwissenschaften, 90, 473–476.

    Article  Google Scholar 

  • Nagashima, H., Sugahara, F., Takechi, M., Ericsson, R., Kawashima-Ohya, Y., Narita, Y., et al. (2009). Evolution of the turtle body plan by the folding and creation of new muscle connections. Science, 325, 193–196.

    Article  Google Scholar 

  • Nagashima, H., Kuraku, S., Uchida, K., Kawashima-Ohya, Y., Narita, Y., & Kuratani, S. (2012). Origin of the turtle body plan—the folding theory to illustrate turtle-specific developmental repatterning. In D. B. Brinkman, P. A. Holroyd, & J. D. Gardner (Eds.) Morphology and evolution of turtles. Dordrecht: Springer.

    Google Scholar 

  • Pritchard, P. C. H. (2008). Evolution and structure of the turtle shell. In J. Wyneken, M. H. Godfrey & V. Bels (Eds.), Biology of Turtles (pp. 45–83). Boca Raton: CRC Press.

    Google Scholar 

  • Procter, J. B. (1922). A study of the remarkable tortoise, Testudo loveridgii Blgr., and the morphogeny of the chelonian carapace. Proceedings of the Zoological Society of London, 3, 483–526.

    Article  Google Scholar 

  • Raff, R. A. (2007). Written in stone: Fossils, genes and evo–devo. Nature Reviews Genetics, 8, 911–920.

    Article  Google Scholar 

  • Reisz, R. R., & Head, J. J. (2008). Turtle origins out to sea. Nature, 456, 450–451.

    Article  Google Scholar 

  • Remane, A. (1952). Die Grundlagen des natürlichen Systems, der vergleichenden Anatomie und der Phylogenetik. Leipzig: Akademische Verlagsgesellschaft Geest & Portig K.-G.

    Google Scholar 

  • Rest, J. S. R., Ast, J. C., Austin, C. C., Waddell, P. J., Tibbetts, E. A., Hay, J. M., et al. (2003). Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome. Molecular Phylogenetics and Evolution, 29, 289–297.

    Article  Google Scholar 

  • Rieppel, O. (2008). The relationships of turtles within amniotes. In J. Wyneken, M. H. Godfrey, & V. Bels (Eds.), Biology of Turtles (pp. 345–353). Boca Raton: CRC Press.

    Google Scholar 

  • Rieppel, O. (2012). The evolution of the turtle shell. In D. B. Brinkman, P. A. Holroyd, & J. D. Gardner (Eds.), Morphology and Evolution of Turtles: Origin and Early Diversification. Dordrecht: Springer.

    Google Scholar 

  • Rieppel, O., & deBraga, M. (1996). Turtles as diapsid reptiles. Nature, 384, 453–455.

    Article  Google Scholar 

  • Rieppel, O., & Reisz, R. R. (1999). The origin and early evolution of turtles. Annual Review of Ecology and Systematics, 30, 1–22.

    Article  Google Scholar 

  • Rubidge, B. S., Modesto, S., Sidor, C., & Welman, J. (1999). Eunotosaurus africanus from the Ecca–Beaufort contact in Northern Cape Province, South Africa—implications for Karoo Basin development. South African Journal of Science, 95, 553–555.

    Google Scholar 

  • Sánchez-Villagra, M. R. (Ed.) (2010). Developmental Vertebrate Palaeontology. Seminars in Cell and Developmental Biology, 21.

    Google Scholar 

  • Sánchez-Villagra, M. R., & Scheyer, T. M. (2010). Fossil turtles from the northern Neotropics: The Urumaco sequence fauna and finds from other localities in Venezuela and Colombia. In M. R. Sánchez-Villagra, O. A. Aguilera & A. A. Carlini (Eds.), Urumaco and Venezuelan Palaeontology—The Fossil Record of the Northern Neotropics (pp. 173–191). Bloomington: Indiana University Press.

    Google Scholar 

  • Sánchez-Villagra, M. R., Müller, H., Sheil, C. A., Scheyer, T. M., Nagashima, H., & Kuratani, S. (2009). Skeletal development in the Chinese soft-shelled turtle Pelodiscus sinensis (Testudines: Trionychidae). Journal of Morphology, 270, 1381–1399.

    Article  Google Scholar 

  • Scheyer, T. M. (2007). Comparative bone histology of the turtle shell (carapace and plastron): Implications for turtle systematics, functional morphology, and turtle origins. Ph.D. Dissertation, Mathematisch-Naturwissenschaftliche Fakultät, University of Bonn, Germany. Available from URN: http://nbn-resolving.de/urn:nbn:de:hbz:5N-12299; URL: http://hss.ulb.uni-bonn.de/diss_online/math_nat_fak/2007/scheyer_torsten.

  • Scheyer, T. M. (2008). Aging the oldest turtles: The placodont affinities of Priscochelys hegnabrunnensis. Naturwissenschaften, 95, 803–810.

    Article  Google Scholar 

  • Scheyer, T. M., & Sander, P. M. (2007). Terrestrial palaeoecology for basal turtles indicated by shell bone histology. Proceedings of the Royal Society of London, B 274, 1885–1893.

    Article  Google Scholar 

  • Scheyer, T. M., & Sander, P. M. (2009). Bone microstructures and mode of skeletogenesis in osteoderms of three pareiasaur taxa from the Permian of South Africa. Journal of Evolutionary Biology, 22, 1153–1162.

    Article  Google Scholar 

  • Scheyer, T. M., Sander, P. M., Joyce, W. G., Böhme, W., & Witzel, U. (2007). A plywood structure in the shell of fossil and living soft-shelled turtles (Trionychidae) and its evolutionary implications. Organisms, Diversity & Evolution, 7, 136–144.

    Article  Google Scholar 

  • Scheyer, T. M., Brüllmann, B., & Sánchez-Villagra, M. R. (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.

    Article  Google Scholar 

  • Schoch, R. R. (2009). Evolution of life cycles in early amphibians. Annual Review of Earth and Planetary Sciences, 37, 135–162.

    Article  Google Scholar 

  • Shaffer, B. S. (2009). Turtles (Testudines). In S. B. Hedges & S. Kumar (Eds.), The Timetree of Life (pp. 398–401). New York: Oxford University Press.

    Google Scholar 

  • Sheil, C. A., & Greenbaum, E. (2005). Reconsideration of skeletal development of Chelydra serpentina (Reptilia: Testudinata: Chelydridae): Evidence for intraspecific variation. Journal of Zoology, London, 265, 235–267.

    Article  Google Scholar 

  • Shubin, N. H., & Alberch, P. (1986). A morphogenetic approach to the origin and basic organization of the tetrapod limb. Evolutionary Biology, 20, 319–387.

    Google Scholar 

  • Shubin, N., Tabin, C., & Carroll, S. (2009). Deep homology and the origins of evolutionary novelty. Nature, 457, 818–823.

    Article  Google Scholar 

  • Sterli, J., de La Fuente, M. S., & Rougier, G. W. (2007). Anatomy and relationships of Palaeochersis talampayensis, a Late Triassic turtle from Argentina. Palaeontographica Abt. A 281, 1–61.

    Google Scholar 

  • Tsuji, L. A., & Müller, J. (2009). Assembling the history of the Parareptilia: Phylogeny, diversification, and a new definition of the clade. Fossil Record, 12, 71–81.

    Article  Google Scholar 

  • Vickaryous, M., & Sire, J. Y. (2009). The integumentary skeleton of tetrapods: Origin, evolution, and development. Journal of Anatomy, 214, 441–464.

    Article  Google Scholar 

  • Werneburg, I. (2009). A standard system to study vertebrate embryos. PLoS ONE, 4(6): e5887. doi:10.1371/journal.pone.0005887.

    Article  Google Scholar 

  • Werneburg, I. (2010). Evolution and Development of Turtles: Organogenesis and Cranial Musculature. Ph.D. Dissertation, Paläontologisches Institut und Museum, Universität Zürich, Schweiz. Scidinge Hall Verlag, Zürich [ISBN: 978-3-905923-03-2].

    Google Scholar 

  • Werneburg, I., & Sánchez-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.

  • Werneburg, I., & Sánchez-Villagra, M. R. (2011). The early development of the echidna, Tachyglossus aculeatus (Mammalia: Monotremata) and patterns of mammalian development. Acta Zoologica (Stockholm), 92, 75–88.

    Article  Google Scholar 

  • Werneburg, I., Hugi, J., Müller, J., & Sánchez-Villagra, M. R. (2009). Embryogenesis and ossification of Emydura subglobosa (Testudines, Pleurodira, Chelidae) and patterns of turtle development. Developmental Dynamics, 238, 2770–2786.

    Article  Google Scholar 

  • Wood, R. C., & Díaz de Gamero, M. L. (1971). Podocnemis venezuelensis, a new fossil pelomedusid (Testudines, Pleurodira) from the Pliocene of Venezuela and a review of the history of Podocnemis in South America. Breviora, 376, 1–23.

    Google Scholar 

  • Ziermann, J. M. (2008). Evolutionäre Entwicklung larvaler Cranialmuskulatur der Anura und der Einfluss von Sequenzheterochronien. Ph.D. Dissertation, Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität, Jena.

    Google Scholar 

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Acknowledgments

We thank Shigeru Kuratani (Kobe), Johannes Müller (Berlin), Uwe Fritz (Dresden), Alan Resetar (Chicago), and Janine M. Ziermann (Jena/Leiden), as well as all of their colleagues, for various help in accessing and studying specimens. Nadia Fröbisch (Chicago), James Gardner (Drumheller), Olivier Rieppel (Chicago), and Matt Vickaryous (Guelph) are thanked for their constructive comments on the manuscript. We also thank all of our collaborators and the SNSF, grant 31003A_127053/1 (to TMS), for supporting this research.

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Scheyer, T.M., Werneburg, I., Mitgutsch, C., Delfino, M., Sánchez-Villagra, M.R. (2013). Three Ways to Tackle the Turtle: Integrating Fossils, Comparative Embryology, and Microanatomy. In: Brinkman, D., Holroyd, P., Gardner, J. (eds) Morphology and Evolution of Turtles. Vertebrate Paleobiology and Paleoanthropology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4309-0_6

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