Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A Middle Triassic stem-turtle and the evolution of the turtle body plan

Subjects

Abstract

The origin and early evolution of turtles have long been major contentious issues in vertebrate zoology1,2,3,4,5,6,7,8,9,10,11. This is due to conflicting character evidence from molecules and morphology and a lack of transitional fossils from the critical time interval. The 220-million-year-old stem-turtle Odontochelys from China12 has a partly formed shell and many turtle-like features in its postcranial skeleton. Unlike the 214-million-year-old Proganochelys from Germany and Thailand, it retains marginal teeth and lacks a carapace. Odontochelys is separated by a large temporal gap from the 260-million-year-old Eunotosaurus from South Africa, which has been hypothesized as the earliest stem-turtle4,5. Here we report a new reptile, Pappochelys, that is structurally and chronologically intermediate between Eunotosaurus and Odontochelys and dates from the Middle Triassic period (240 million years ago). The three taxa share anteroposteriorly broad trunk ribs that are T-shaped in cross-section and bear sculpturing, elongate dorsal vertebrae, and modified limb girdles. Pappochelys closely resembles Odontochelys in various features of the limb girdles. Unlike Odontochelys, it has a cuirass of robust paired gastralia in place of a plastron. Pappochelys provides new evidence that the plastron partly formed through serial fusion of gastralia3,13. Its skull has small upper and ventrally open lower temporal fenestrae, supporting the hypothesis of diapsid affinities of turtles2,7,8,9,10,14,15.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: P. rosinae.
Figure 2: Skull elements of P. rosinae (digitally extracted from surrounding matrix).
Figure 3: Postcranial elements of P. rosinae (digitally extracted from surrounding matrix).
Figure 4: Phylogenetic position of Pan-Testudines including Pappochelys among Amniota based on maximum parsimony analysis of the data matrix in ref. 5.
Figure 5: Early evolution of the turtle body plan.

References

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

    CAS  Article  Google Scholar 

  2. Rieppel, O. & Reisz, R. R. The origin and early evolution of turtles. Annu. Rev. Ecol. Syst. 30, 1–22 (1999)

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  5. Lyson, T. R., Bever, G. S., Scheyer, T. M., Hsiang, A. Y. & Gauthier, J. A. Evolutionary origin of the turtle shell. Curr. Biol. 23, 1113–1119 (2013)

    CAS  Article  Google Scholar 

  6. Rieppel, O. in Morphology and Evolution of Turtles (eds Brinkman, D. B., Holroyd, P. A. & Gardner, J. D. ) 51–61 (Springer, 2013)

    Book  Google Scholar 

  7. Hedges, S. B. & Poling, L. L. A molecular phylogeny of reptiles. Science 283, 998–1001 (1999)

    ADS  CAS  Article  Google Scholar 

  8. Crawford, N. G. et al. More than 1000 ultraconserved elements provide evidence that turtles are the sister group of archosaurs. Biol. Lett. 8, 783–786 (2012)

    Article  Google Scholar 

  9. Lee, M. S. Y. Turtle origins: insights from phylogenetic retrofitting and molecular scaffolds. J. Evol. Biol. 26, 2729–2738 (2013)

    CAS  Article  Google Scholar 

  10. Lu, B., Yang, W., Dai, Q. & Fu, J. Using genes as characters and a parsimony analysis to explore the phylogenetic position of turtles. PLoS ONE 8, e79348 (2013)

    ADS  Article  Google Scholar 

  11. Hirasawa, T., Pascual-Anaya, J., Kamezaki, N., Taniguchi, M., Mine, K. & Kuratani, S. The evolutionary origin of the turtle shell and its dependence on the axial arrest of the embryonic rib cage. J. Exp. Zool. B 324, 194–207 (2015)

    Article  Google Scholar 

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

    ADS  CAS  Article  Google Scholar 

  13. Zangerl, R. The homology of the shell elements in turtles. J. Morphol. 65, 383–406 (1939)

    Article  Google Scholar 

  14. deBraga, M. & Rieppel, O. Reptile phylogeny and the affinities of turtles. Zool. J. Linn. Soc. 120, 281–354 (1997)

    Article  Google Scholar 

  15. Müller, J. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Wilson, M. V. H. & Cloutier, R. ) 379–408 (Dr Friedrich Pfeil, 2004)

    Google Scholar 

  16. Joyce, W. G., Parham, J. F. & Gauthier, J. A. Developing a protocol for the conversion of rank-based taxon names to phylogenetically defined clade names, as exemplified by turtles. J. Paleontol. 78, 989–1013 (2004)

    Article  Google Scholar 

  17. Schoch, R. R. Stratigraphie und Taphonomie wirbeltierreicher Schichten im Unterkeuper (Mitteltrias) von Vellberg (SW-Deutschland). Stuttgart. Beitr. Naturk. B 318, 1–30 (2002)

    Google Scholar 

  18. Gaffney, E. S. The comparative osteology of the Triassic turtle Proganochelys. Bull. Am. Mus. Nat. Hist. 194, 1–263 (1990)

    Google Scholar 

  19. Watson, D. M. S. Eunotosaurus africanus Seeley, and the ancestry of the Chelonia. Proc. Zool. Soc. Lond. 1914, 1011–1020 (1914)

    Google Scholar 

  20. Li, C., Yang, D.-Y., Cheng, L., Wu, X.-C. & Rieppel, O. A new species of Largocephalosaurus (Diapsida: Saurosphargidae), with implications for the morphological diversity and phylogeny of the group. Geol. Mag. 151, 100–120 (2014)

    ADS  Article  Google Scholar 

  21. Hirasawa, T., Nagashima, H. & Kuratani, S. The endoskeletal origin of the turtle carapace. Nat. Commun. 4, 2107 (2013)

    ADS  Article  Google Scholar 

  22. Gow, C. E. A reassessment of Eunotosaurus africanus Seeley (Amniota: Parareptilia). Palaeont. Afr. 34, 33–42 (1997)

    Google Scholar 

  23. Bever, G. S., Lyson, T. & Bhullar, B.-A. Fossil evidence for a diapsid origin of the anapsid turtle skull. Soc. Vert. Paleont. Abstr. 2014, 91 (2014)

    Google Scholar 

  24. Joyce, W. G. & Gauthier, J. A. Palaeoecology of Triassic stem turtles sheds new light on turtle origins. Proc. R. Soc. Lond. B 271, 1–5 (2003)

    Article  Google Scholar 

  25. Scheyer, T. M. & Sander, P. M. Shell bone histology indicates terrestrial palaeoecology of basal turtles. Proc. R. Soc. B 274, 1885–1893 (2007)

    Article  Google Scholar 

Download references

Acknowledgements

We acknowledge the Schumann family for their continued support and granting access to the Vellberg quarry, and F. Ullmann, B. Rozynek, W. Kugler, T. Haubold, U. Günter, and M. Salomon for assistance in the field and for donating specimens to the Staatliches Museum für Naturkunde Stuttgart. N. Klein and T. Scheyer assisted with the histological interpretation of the thin-sections. T. Lyson provided the character-taxon matrix used in ref. 5. I. Rosin, N. Adorf, M. Kamenz, and K. Krämer prepared the material, and C. Wimmer-Pfeil prepared thin-sections. We thank D. Seegis, H. Hagdorn, W. Joyce, N. Klein, T. Lyson, J. Müller, O. Rieppel, and T. Scheyer for discussions.

Author information

Authors and Affiliations

Authors

Contributions

R.R.S. and H.-D.S. contributed equally to the research and the development of the manuscript; therefore their names are listed in alphabetical order.

Corresponding authors

Correspondence to Rainer R. Schoch or Hans-Dieter Sues.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

P. rosinae is in the ZooBank database (http://zoobank.org/) with Life Science Identifier urn:lsid:zoobank.org:act:CDD54976-047F-43AA-80F4-9680DF78CD7B.

Extended data figures and tables

Extended Data Figure 1 Cranial material of P. rosinae.

a, b, Photograph and explanatory outline drawing of partial skull and postcranial skeleton of P. rosinae (SMNS 91356); c, left parietal in ventral view; d, right parietal in dorsal view; e, left postorbital; f, left postfrontal; g, left frontal. Abbreviations: dv, dorsal vertebra; f, frontal; ga, gastralium; j, jugal; mt, metatarsal; n, nasal; p, parietal; ph, phalanx; po, postorbital; pof, postfrontal; ti, tibia; tv, tail vertebra.

Extended Data Figure 2 Skeletal remains of a very small individual of P. rosinae.

a, b, Photograph (a) and explanatory outline drawing (b) of associated skeletal remains of a very small individual of P. rosinae (SMNS 92066). Bones of the skull are shown in a darker shade of grey. Abbreviations: d, dentary; dv, dorsal vertebra; fe, femur; gas, gastralia; j, jugal; prf, prefrontal; pt?, possible pterygoid; ti, tibia.

Extended Data Figure 3 Gastralia of P. rosinae.

a, b, Photograph (a) and explanatory outline (b) of a set of gastralia elements and fragments of two trunk ribs (black) that are part of the incomplete, partly articulated postcranial skeleton SMNS 91360.

Extended Data Figure 4 Transverse section through the broadened shaft of a left trunk rib.

Extended Data Figure 5 Tree illustrating hypothesis of turtle relationships based on the Tree Analysis using New Technology (TNT) program.

Individual nodes are numbered. For additional information refer to ‘Phylogenetic analysis’ section in Supplementary Information.

Extended Data Figure 6 Tree illustrating hypothesis of turtle relationships based on Bayesian analysis.

Numbers at individual nodes represent posterior probabilities. For additional information refer to ‘Phylogenetic analysis’ section in Supplementary Information.

Supplementary information

Supplementary information

This file contains additional specimen and locality data, a list of characters and character-states, information on phylogenetic analysis and additional morphological detail on trunk ribs. (PDF 599 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schoch, R., Sues, HD. A Middle Triassic stem-turtle and the evolution of the turtle body plan. Nature 523, 584–587 (2015). https://doi.org/10.1038/nature14472

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature14472

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing