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 Triassic stem turtle with an edentulous beak

Abstract

The early evolution of turtles continues to be a contentious issue in vertebrate palaeontology. Recent reports have suggested that they are diapsids1,2,3,4,5,6, but the position of turtles within Diapsida is controversial7,8,9,10,11,12 and the sequence of acquisition of turtle synapomorphies remains unclear1,2,3. Here we describe a Triassic turtle from China that has a mixture of derived characters and plesiomorphic features. To our knowledge, it represents the earliest known stem turtle with an edentulous beak and a rigid puboischiadic plate. The discovery of this new form reveals a complex early history of turtles.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The holotype of E. sinensis (SMMP 000016).
Fig. 2: Skull of E. sinensis (SMMP 000016).
Fig. 3: Posterior dorsal vertebrae and pelvic girdle of stem turtles.
Fig. 4: Phylogenetic position of Eorhynchochelys among amniotes.

Similar content being viewed by others

References

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

    Google Scholar 

  2. Schoch, R. R. & Sues, H.-D. A Middle Triassic stem-turtle and the evolution of the turtle body plan. Nature 523, 584–587 (2015).

    Article  ADS  PubMed  CAS  Google Scholar 

  3. Bever, G. S., Lyson, T. R., Field, D. J. & Bhullar, B.-A. Evolutionary origin of the turtle skull. Nature 525, 239–242 (2015).

    Article  ADS  PubMed  CAS  Google Scholar 

  4. Schoch, R. R. and Sues, H.-D. Osteology of the Middle Triassic stem-turtle Pappochelys rosinae and the early evolution of the turtle skeleton. J. Syst. Palaeontol. 16, 927–965 (2017).

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  ADS  PubMed  CAS  Google Scholar 

  8. 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  PubMed  PubMed Central  Google Scholar 

  9. 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).

    Article  PubMed  CAS  Google Scholar 

  10. Rieppel, O. in Morphology and Evolution of Turtles (eds Brinkman, D. B. et al.) 51–61 (Springer, Dordrecht, 2013).

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

    Article  PubMed  CAS  Google Scholar 

  12. Hirasawa, T. et al. The evolutionary origin of the turtle shell and its dependence on the axial arrest of the embryonic rib cage. J. Exp. Zool. B Mol. Dev. Evol. 324, 194–207 (2015).

    Article  PubMed  Google Scholar 

  13. 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).

    Article  ADS  PubMed  CAS  Google Scholar 

  14. Joyce, W. G. & Gauthier, J. A. Palaeoecology of Triassic stem turtles sheds new light on turtle origins. Proc. R. Soc. B 271, 1–5 (2004). 

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  16. Goloboff, P., Farris, J. & Nixon, K. TNT. A free program for phylogenetic analysis. Cladistics 24, 774–786 (2008).

    Article  Google Scholar 

  17. Lyson, T. R. et al. Fossorial origin of the turtle shell. Curr. Biol. 26, 1887–1894 (2016).

    Article  PubMed  CAS  Google Scholar 

  18. Jenkins, F. A. Jr. Anatomy and function of expanded ribs in certain edentates and primates. J. Mamm. 51, 288–301 (1970).

    Article  Google Scholar 

  19. Fraser, N. C. Palaeontology: a hook to the past. Curr. Biol. 26, R922–R925 (2016).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Z.-Y. Sun and Sanya Museum of Marine Paleontology for access to the specimen, J.-Z. Ding (IVPP) for skilful preparation of the specimen, W. Gao (IVPP) for photographic assistance, Y.-S. Lou (IVPP) for laboratory assistance during the course of the study, L.-T. Wang (Guizhou Geological Survey) for field assistance, and R.R. Schoch, H.-D. Sues, G.S. Bever and T.R. Lyson for providing information or references. X.-C.W., N.F. and O.R. thank the IVPP for hospitality during their visits. This work was supported by the Strategic Priority Research Programs of Chinese Academy of Sciences (XDA19050102 and XDB26000000 to C.L.), the National Science Foundation of China (41772006 to C.L.) together with support from the IVPP and the Canadian Museum of Nature (RCP09 to X.-C.W.).

Reviewer information

Nature thanks G. S. Bever, R. R. Schoch and H.-D. Sues for their contribution to the peer review of this work.

Author information

Authors and Affiliations

Authors

Contributions

All authors conceived the project and participated in the writing of the text and Supplementary Information. C.L. led the field work and acquired the specimen for study. X.-C.W. drafted the figures with input from all authors.

Corresponding authors

Correspondence to Chun Li or Xiao-Chun Wu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Stratigraphic section of the Lower Wayao Member (LWM) of the Falang Formation.

The section was found at Heshangjing, Baiyuncun of Xinpuxiang in Guanling of Guizhou Province, near the locality of E. sinensis. The Guanling biota originates in the lower part of the upper unit in the LWM. The LWM is about 14.5 m thick in this section, nearly 2.5 m thicker than that of the Wolonggang quarry section near the village of Xiaowa (Supplementary Information). The block of the black shaly marlstone containing E. sinensis is full of small bivalves, whereas the block of thin marlstones containing O. semitestacea has large bivalves (species of Halobia and Daonella) and also scattered ammonites (species of Trachyceras and Paratrachyceras). The horizon where E. sinensis originated is 7.5 m below the one that contained O. semitestacea but slightly above the dark grey, marly, laminated micritic limestones that produce abundant skeletons of ichthyosaurs, thalattosaurs and placodonts as well as other fossils (Supplementary Information).

Extended Data Fig. 2 Extra information on the skull of E. sinensis (SMMP 000016).

a, b, X-radiograph and photograph of the skull in ventral view. c, d, Photograph and line drawing of the snout portion of the skull in right-lateral view, showing the ornamentation on the external surface of the edentulous premaxillae, the anterior portions of the right dentary and maxilla; the absence of teeth and the surface ornamentation suggest the presence of a rhamphotheca in E. sinensis in life. e, Close-up photograph of the posterior portion of the left maxilla, showing column-like pleurodont posterior teeth with blunt tips and the teeth deeply inset from the labial margin and ankylosed to the labial base, which differs from the subthecodont implantation in Eunotosaurus africanus and Pappochelys rosinae; the implantation pattern of the teeth is unknown for O. semitestacea, because the lingual side of the dentition is not exposed in the known specimens. New characters: ch. 273 (1), keratinous beak present, as indicated by surface ornamentation; ch. 274 (1), anterior end of the dentary edentulous; ch. 275 (1), dentary tooth number fewer than 30. d, dentary; l, lacrimal; m, maxilla; ob, orbit; pm, premaxilla.

Extended Data Fig. 3 A close-up of the postorbital portion of the skull roof of E. sinensis (SMMP 000016) in dorsal view.

a, Photograph. b, Line drawing, showing no supratemporal or trace of a supratemporal fenestra between the frontal, postfrontal, postorbital and parietal. Zigzag lines denote broken surfaces. f, frontal; j, jugal; lp, left parietal; ltf, lower temporal fenestra; ob, orbit, po, postorbital; pof, postfrontal; rp, right parietal; sq, squamosal.

Extended Data Fig. 4 Cervical and dorsal vertebrae of E. sinensis (SMMP 000016).

a, b, Axis and cervical 3 in dorsal and left-lateral views, showing that the axis is characterized by an anteroposteriorly broadened neural spine that is higher posteriorly than anteriorly, unlike Proganochelys quenstedti and other turtles that show an anterior midline projection on the axis neural spine. c, d, Dorsals 6 and 7 in dorsal view, showing the prezygapophyses and postzygapophyses that are unusually different in size, unlike those of the post-axial cervicals and the first two dorsal vertebrae that are similar in size and robustness. e, An incomplete osteoderm in dorsal view. There is no evidence of extensive dermal armour. The single fragment of an osteoderm with surface ornamentation located between the transverse processes of the fourth and fifth caudal vertebrae is, however, inconsistent with the otherwise excellent preservation and articulation of the skeleton and almost certainly represents a different taxon and individual. Zigzag lines denote broken surfaces. atc, atlantal centrum; ax, axis; cap, capitulum; cav4, caudal vertebra 4; cv3, cervical vertebra 3; dv7, dorsal vertebra 7; ns, neural spine; nt, neural table; os, osteoderm; poz, postzygapophysis; prz, prezygapophysis; r, rib; rh, rib head; tub, tuberculum.

Extended Data Fig. 5 Posterior trunk of E. sinensis (SMMP 000016) in dorsal view.

a, Photograph. b, Line drawing showing that the dorsal surface of the distinctly broadened dorsal ribs is faintly ornamented by a series of striations. In addition, the stout sacral ribs are fused to the sacral vertebrae (as they are in O. semitestacea and P. rosinae) and their distinctly expanded distal ends are detached from the ilium, in contrast to the tightly fused condition in P. quenstedti. Dorsal ribs 11 and 12 of E. sinensis are not specialized and are very different from dorsal ribs 1–9 in morphology.

Extended Data Fig. 6 Puboischiadic plate in stem turtles.

ac, Photograph, line drawing and reconstruction of the puboischiadic plate of E. sinensis (SMMP 000016) in ventral view. d, e, Photograph and line drawing of the puboischiadic plate of O. semitestacea (the paratype, IVPP V 13240) with the ossified hypoischium in ventral view. New characters: ch. 276 (1), lateral process of the ischium present; ch. 277 (1), posterior directed process of the ischium present; ch. 278 (1), bony symphysis (a sutural midventral contact) between pubes and ischia present; ch. 279 (1), the rigid puboischiadic plate with a ventromidline keel present in adults; ch. 280 (1), hypoischium present. fem;, femur; his, hypoischium; is, ischium; lppu, lateral process of the pubis; ltis, lateral tubercle of the ischium; of, obturator foramen; peis; posterior elongation of the ischium; pik, puboischiadic keel; plt, plastron; pu, pubis.

Extended Data Fig. 7 Strict consensus of 16 most parsimonious trees.

The 16 trees (with a tree length of 1,207, a consistency index of 0.269, and a retention index of 0.582) were generated using a new technology search of TNT v.1.016 based on the large data matrix (52 taxa and 280 characters) derived from previously published datasets3,4, showing that the monophyly of ‘Pantestudines’ with Claudiosaurus and Acerosodontosaurus excluded and the interrelationships of Eorhynchochelys within the clade are the same as produced by the analysis based on the reduced dataset4 (see the clade formed by Eunotosaurus and more derived turtles in Fig. 4). As in the analysis of the reduced dataset, the new technology search based on 100 random addition sequence replicates and 1,000 random seeds was implemented, and the advanced search settings were changed to ensure enough iterations: 100 sectorial search drifting cycles, 100 ratchet iterations, 100 drift cycles and 100 rounds of tree fusion for every replicate. Multistate characters were treated as unordered and all characters were equally weighted. Bremer supporting values (numbers) are shown for each node.

Supplementary information

Supplementary Information

This file contains Supplementary Data sections 1-3 and Supplementary References.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, C., Fraser, N.C., Rieppel, O. et al. A Triassic stem turtle with an edentulous beak. Nature 560, 476–479 (2018). https://doi.org/10.1038/s41586-018-0419-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-018-0419-1

This article is cited by

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