Skip to main content

The Evolution of the Turtle Shell

  • Chapter
  • First Online:
Morphology and Evolution of Turtles

Part of the book series: Vertebrate Paleobiology and Paleoanthropology ((VERT))

Abstract

This chapter traces the history of the debate on the evolution of the turtle shell, and carries the analysis of the origin of the turtle carapace forward from two complementary perspectives, viz. paleontology and developmental biology. Two alternative approaches to morphological analysis—the transformationist and the emergentist—are identified. The transformationist approach seeks to understand morphological evolution as a consequence of the gradual, step-wise transformation of the adult phenotype. The emergentist approach allows for ontogenetic deviation to result in the development of evolutionary novelties. The discovery of the so far oldest and most primitive turtle known, from the early Late Triassic of southwestern China, provides the basis for a synthesis of paleontological and developmental data in the understanding of the evolutionary origin of the turtle shell.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 119.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Baur, G. (1886). Osteologische Notizen über Reptilien. Zoologischer Anzeiger, 9, 685–690.

    Google Scholar 

  • Baur, G. (1887). On the morphogeny of the carapace of the Testudinata. The American Naturalist, 21, 89.

    Google Scholar 

  • Baur, G. (1888). Unusual dermal ossifications. Science, 11, 144–145.

    Article  Google Scholar 

  • Baur, G. (1889). Die systematische Stellung von Dermochelys Blainv. Biologisches Zentralblatt, 9, 149–153.

    Google Scholar 

  • Burke, A. C. (1989a). Critical feature in chelonian development: The ontogeny and phylogeny of a unique tetrapod bauplan. Ph.D Dissertation, Harvard University, Cambridge, MA.

    Google Scholar 

  • Burke, A. C. (1989b). Development of the turtle carapace: Implications for the evolution of a novel bauplan. Journal of Morphology, 199, 363–378.

    Article  Google Scholar 

  • Burke, A. C. (1991). The development and evolution of the turtle body plan: Inferring intrinsic aspects of the evolutionary process from experimental embryology. American Zoologist, 31, 616–627.

    Google Scholar 

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

    Article  Google Scholar 

  • Carroll, R. L. (1988). Vertebrate Paleontology and Evolution. New York: W. H. Freeman.

    Google Scholar 

  • Carus, K. G. (1834). Lehrbuch der Vergleichenden Zootomie. 2. Aufl., Bd. I. . Leipzig: Ernst Fleischer.

    Google Scholar 

  • Case, E. C. (1898). Toxochelys. University of Kansas Geological Survey, 4, 370–385.

    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 in the turtle Trachemys scriptascripta. Evolution & Development, 9, 267–277.

    Article  Google Scholar 

  • Cebra-Thomas, J. A., Tan, F., Sistla, S., Estes, E., Bender, G., Kim, C., Riccio, P., & Gilbert, S. F. (2005). How the turtle forms its shell: A paracrine hypothesis of carapace formation. Journal of Experimental Zoology (Mol Dev Evol), 304B, 558–569.

    Article  Google Scholar 

  • Clark, K., Bender, G., Murray, B. P., Panfilio, K., Cook, S., Davis, R., Murnen, K., Tuan, R. S., & Gilbert, S. F. (2001). Evidence for the neural crest origin of turtle plastron bones. Genesis, 3, 111–117.

    Article  Google Scholar 

  • Cope, E. D. (1871). On the homologies of some of the cranial bones of the Reptilia, and the systematic arrangement of the class. In Proceedings of the American Association for the Advancement of Science, (pp. 194–247).

    Google Scholar 

  • Cuvier, G. (1799). Leçons d’Anatomie Comparée, Vol. I. Paris: Boudouin.

    Google Scholar 

  • Cuvier, G. (1812). Recherches sur les Ossements Fossiles de Quadrupèdes, Vol. IV. Paris: Deterville.

    Google Scholar 

  • Darwin, Ch. (1859). On the Origin of Species. London: John Murray.

    Google Scholar 

  • Dollo, L. (1886). Première note sur les chéloniens du Bruxellien (Eocène moyen) de la Belgique. Bulletin du Musée Royale d’Histoire Naturelle de la Belgique, 4, 75–96.

    Google Scholar 

  • 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 

  • Gauthier, J. A. (1994). The diversification of amniotes. In D. Prothero, & R. M. Schoch (Eds.), Major Features of Vertebrate Evolution (pp. 129–159). Knoxville: Paleontological Society.

    Google Scholar 

  • Geoffroy, S-H. E. (1818). Philosophie Anatomique. Des Organes Respiratoires sous le Rapport de la Détermination et de l’Identité de leurs Pièces Osseuses. I. J.B. Baillière: Paris.

    Google Scholar 

  • Gervais, P. (1872). Ostéologie du Sphargis Luth (Sph. coriacea). Nouveau Archives du Muséum d’Histoire Naturelle, Paris, 8, 199–228.

    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 

  • Gilbert, S. F., Cebra-Thomas, J. A., & Burke, A. C. (2008). How the turtle gets its shell. In J. Wyneken, M. H. Godfrey & V. Bels (Eds.), Biology of Turtles (pp. 1–16). Boca Raton: CRC Press.

    Google Scholar 

  • Goette, A. (1899). Über die Entwicklung des knöchernen Rückenschildes (Carapax) der Schildkröten. Zeitschrift für wissenschaftliche Zoologie, 66, 407–434.

    Google Scholar 

  • Haines, R. W., & Mohuiddin, A. (1968). Metaplastic bone. Journal of Anatomy, 103, 527–538.

    Google Scholar 

  • Hay, O. P. (1898). On Protostega, the systematic position of Dermochelys, and the morphogeny of the chelonian carapace and plastron. American Naturalist, 32, 929–948.

    Article  Google Scholar 

  • Hay, O.P. (1905). On the group of fossil turtles known as Amphichelydia; with remarks on the origin and relationships of the suborders, superfamilies, and families of Testudines. Bulletin of the American Museum of Natural History, 21, 137–175.

    Google Scholar 

  • Hay, O. P. (1908). The Fossil Turtles of North America. Washington DC: Carnegie Institution.

    Book  Google Scholar 

  • Hay, O. P. (1922). On the phylogeny of the shell of the Testudinata and the relationships of Dermochelys. Journal of Morphology, 36, 421–445.

    Article  Google Scholar 

  • Hay, O. P. (1928). Further consideration of the shell of Chelys and of the constitution of the armor of turtles in general. In Proceedings of the U.S. National Museum, 73, pp.1–12.

    Google Scholar 

  • Haycraft, J. B. (1891). The development of the carapace of the Chelonia. Transactions of the Royal Society of Edinburgh, 36, 335–342.

    Article  Google Scholar 

  • Henderson, D. M. (2003). Effects of stomach stones on the buoyancy and equilibrium of a floating crocodilian: A computational analysis. Canadian Journal of Zoology, 81, 1346–1357.

    Article  Google Scholar 

  • Henderson, D. M. (2006). Floating point: A computational study of buoyancy, equilibrium, and gastroliths in plesiosaurs. Lethaia, 39, 227–244.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hoffmann, C. K. (1878). Beiträge zur vergleichenden Anatomie der Wirbelthiere. Tafel IX –XIII. Niederländisches Archiv für Zoologie, 4, 112–248.

    Google Scholar 

  • Jollie, M. (1962). Chordate Morphology. New York: Reinhold.

    Book  Google Scholar 

  • Joyce, W. J. (2007). Phylogenetic relationships of Mesozoic turtles. Bulletin of the Peabody Museum of Natural History, 48, 3–102.

    Article  Google Scholar 

  • Joyce, W. G., & Gauthier, J. A. (2003). Paleoecology of Triassic stem turtles sheds new light on turtle origins. In Proceedings of the Royal Society of London B, 271, pp. 1–5.

    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. In Proceedings of the Royal Society of London B, 276, 507–513.

    Google Scholar 

  • Kälin, J. (1945). Zur Morphogenese des Panzers bei den Schildkröten. Acta Anatomica, 1, 144–176.

    Article  Google Scholar 

  • Kordikova, E. G. (2000). Paedomorphosis in the shell of fossil and living turtles. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen, 218, 399–446.

    Google Scholar 

  • Kordikova, E. G. (2002). Heterochrony in the evolution of the shell of Chelonia. Part 1. Terminology, Cheloniidae, Dermochelyidae, Trionychidae, Cyclanorbidae and Carettochelyidae. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen, 226, 343–417.

    Google Scholar 

  • Kuraku, S., Usuda, R., & Kuratani, S. (2005). Comprehensive survey of carapacial ridge-specific genes in turtle implies co-option of some regulatory genes in carapace evolution. Evolution & Development, 7, 3–17.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lee, M. S. Y. (1993). The origin of the turtle body plan: bridging a famous morphological gap. Science, 261, 1716–1720.

    Article  Google Scholar 

  • Lee, M. S. Y. (1996). Correlated progression and the origin of turtles. Nature, 379, 811–815.

    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 

  • Menger, W. (1922). Ontogenie und Phylogenie des Schildkrötenpanzers. Ph.D. Dissertation, Hessische Ludwigs-Universität, Giessen.

    Google Scholar 

  • Merrem, B. (1820). Versuch eines Systems der Amphibien. Tentamen sistematis amphibiorum. Marburg.

    Book  Google Scholar 

  • Meyer, H.v. (1847). Mittheilungen an Professor Bronn gerichtet. Neues Jahrbuch für Mineralogie, Geognosie, Geologie, und Petrefakten-Kunde, 1847, 572–580.

    Google Scholar 

  • Meyer, H. v. (1858). Psephoderma alpinum aus dem Dachsteinkalke der Alpen. Palaeontographica, 6, 246–252.

    Google Scholar 

  • Moss, M. L. (1969). Comparative histology of dermal sclerifications in reptiles. Acta Anatomica, 73, 510–533.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Newman, H. H. (1905–1906). The significance of scute and plate “Abnormalities” in Chelonia. Biological Bulletin, 10, 68–114.

    Google Scholar 

  • Nagashima, H., Kuraku, S., Uchida, K., Kawashima-Ohya, Y., Narita, Y., & Kuratani, S. (2007). On the carapacial ridge in turtle embryos: Its developmental origin, function and the chelonian body plan. Development, 134, 2219–2226.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Nosotti, S., & Pinna, G. (1989). Storia delle ricerche e degli studi sui rettili placodonti. Memorie della Società Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano, 24, 29–86.

    Google Scholar 

  • Oguschi, K. (1911). Anatomische Studien an der japanischen dreikralligen Lippenschildkröte (Trionyx japanicus). Gegenbaurs Morphologisches Jahrbuch, 43, 1–106.

    Google Scholar 

  • Owen, R. (1849). On the development of the carapace and plastron of the chelonian reptiles. Philosophical Transactions of the Royal Society of London, 139, 151–171.

    Article  Google Scholar 

  • Patterson, C. (1977). Cartilage bones, dermal bones and membrane bones, or the exoskeleton versus the endoskeleton. In S. M. Andrews, R. S. Miles & A. D. Walker (Eds.), Problems in Vertebrate Evolution (pp. 77–121). London: Academic Press.

    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 the 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. In Proceedings of the Zoological Society of London, 92, 483–526.

    Google Scholar 

  • Rathke, H. (1848). Uber die Entwicklung der Schildkröten. Braunschweig: Friedrich Vieweg und Sohn.

    Book  Google Scholar 

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

    Article  Google Scholar 

  • Rieppel, O. (2001). Turtles as hopeful monsters. BioEssays, 23, 987–991.

    Article  Google Scholar 

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

    Google Scholar 

  • Rieppel, O., & Kearney, M. (2007). The poverty of taxonomic characters. Biology & Philosophy, 22, 95–113.

    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 

  • Ruckes, H. (1929). Studies in chelonian osteology. Part II. The morphological relationships between girdles, ribs and carapace. Annals of the New York Academy of Sciences, 31, 81–120.

    Article  Google Scholar 

  • Sánchez-Villagra, M. R., Müller, H., Scheil, 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 

  • Shearman, R. M., & Burke, A. C. (2009). The lateral somatic frontier in ontogeny and phylogeny. Journal of Experimental Biology (Mol Dev Evol), 312B, 603–612.

    Article  Google Scholar 

  • Scheil, A. A. (2003). Osteology and skeletal development of Apalone spinifera (Reptilia: Testudines: Trionychidae). Journal of Morphology, 256, 42–78.

    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 

  • Smith, M. M., & Hall, B. K. (1990). Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biological Reviews, 65, 277–373.

    Article  Google Scholar 

  • Smith, M. M., & Hall, B. K. (1993). A developmental model for the evolution of vertebrate exoskeleton and teeth: the role of cranial and trunk neural crest. Evolutionary Biology, 27, 387–448.

    Google Scholar 

  • Starck, D. (1955). Embryologie. Stuttgart: Georg Thieme.

    Google Scholar 

  • Starck, D. (1979). Vergleichende Anatomie der Wirbeltiere, Bd. 2. Berlin: Springer.

    Google Scholar 

  • Strauch, A. (1890). Bemerkungen über die Schildkrröten-sammlung im Zoologischen Museum der kaiserlichen Akademie der Wissenschaften zu St. Petersburg. Mémoires de l’Académie Impériale des Sciences, St. Petersburg, (7) 38, 1–127.

    Google Scholar 

  • Taylor, A. M. (1993). Stomach stones for feeding or buoyancy? The occurrence and function of gastroliths in marine tetrapods. Philosophical Transactions of the Royal Society of London B, 341, 163–175.

    Article  Google Scholar 

  • Taylor, A. M. (1994). Stone, bone or blubber? Buoyancy control strategies in aquatic tetrapod. In L. Maddock, Q. Bone & J. M. V. Rayner (Eds.), Mechanics and Physiology of Animal Swimming (pp. 151–161). Cambridge UK: Cambridge University Press.

    Chapter  Google Scholar 

  • Taylor, A. M. (2000). Functional significance of bone ballast in the evolution of buoyancy control strategies by aquatic tetrapods. Historical Biology, 14: 15–31.

    Article  Google Scholar 

  • Taylor, A. M. (2002). Origin of marine mammals. In W. F. Perrin, B. Würsig, & J. G. M. Thewissen (Eds.), Encyclopedia of Marine Mammals (pp. 833–837). San Diego: Academic Press.

    Google Scholar 

  • Vallén, E. (1942). Beiträge zur Kenntnis der Ontogenie und der vergleichenden Anatomie des Schildkrötenpanzers. Acta Zoologica, Stockholm, 23, 1–127.

    Article  Google Scholar 

  • Versluys, J. (1914). Über die Phylogenie des Panzers der Schildkröten und über die Verwandtschaft der Lederschildkröte (Dermochelys coriacea). Paläontologische Zeitschrift, 1, 321–347.

    Article  Google Scholar 

  • Vickaryous, M. K., & Hall, B. K. (2008). Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms. Journal of Morphology, 260, 398–422.

    Article  Google Scholar 

  • Völker, H. (1913). Über das Stamm, Gliedmassen-, und Hautskelett von Dermochelys coriacea L. Zoologische Jahrbücher, Abteilung für Anatomie und Ontogenie der Tiere, 33, 431–552.

    Google Scholar 

  • Wang, X., Bachmann, G. H., Hagdorn, H., Sander, P. M., Cuny, G., Chen, X., et al. (2008). The Late Triassic black shales from the Guanling area, Guizhou Province, south-west China: A unique marine reptile and pelagic crinoid fossil Lagerstätte. Palaeontology, 51, 27–61.

    Article  Google Scholar 

  • Wiedeman, C. R. W. (1802). Anatomische Beschreibung der Schildkröten überhaupt und der getäfelten Schildkröte (T. tesselata Schneid., T. tabulata Walbaum) insbesondere. Archiv für Zoologie und Zootomie, 2, 177–210.

    Google Scholar 

  • Wieland, G. R. (1896). Archelon ischyrios: A new gigantic Cryptodire Testudinate from Fort Pierre Cretaceous of South Dakota. American Journal of Science, 2(4), 399–415.

    Article  Google Scholar 

  • Wieland, G. R. (1905). On marine turtles. American Journal of Science, 20, 325–343.

    Article  Google Scholar 

  • Wieland, G. R. (1909). Revision of the Protostegidae. American Journal of Science, 27(4), 237–251.

    Google Scholar 

  • Wings, O. (2007). A review of gastrolith function with implications for fossil vertebrates and a revised classification. Acta Palaeontologica Polonica, 52: 1–16.

    Google Scholar 

  • Yntema, C. L. A. (1968). A series of stages in the embryonic development of Chelydra serpentina. Journal of Morphology, 125, 219–252.

    Article  Google Scholar 

  • Zangerl, R. (1939). The homology of the shell elements in turtles. Journal of Morphology, 65, 383–406.

    Article  Google Scholar 

  • Zangerl, R. (1969). The turtle shell. In C. Gans, A. d’A. Bellairs, & T. S. Parsons (Eds.), Biology of the Reptilia, (Vol. 1). Morphology A (pp. 311–339). London: Academic Press.

    Google Scholar 

Download references

Acknowledgments

I thank Anne Burke, Robert L. Carroll, Hiroshi Nagashima, Torsten M. Scheyer, Michael A. Taylor, and Matthew K. Vickaryous, who all offered helpful comments on an earlier draft of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Olivier Rieppel .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Rieppel, O. (2013). The Evolution of the Turtle Shell. 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_5

Download citation

Publish with us

Policies and ethics