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Evolutionary origin of the turtle skull

Naturevolume 525, pages239–242 (2015)Cite this article

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Abstract

Transitional fossils informing the origin of turtles are among the most sought-after discoveries in palaeontology1,2,3,4,5. Despite strong genomic evidence indicating that turtles evolved from within the diapsid radiation (which includes all other living reptiles6,7), evidence of the inferred transformation between an ancestral turtle with an open, diapsid skull to the closed, anapsid condition of modern turtles remains elusive. Here we use high-resolution computed tomography and a novel character/taxon matrix to study the skull ofEunotosaurus africanus, a 260-million-year-old fossil reptile from the Karoo Basin of South Africa, whose distinctive postcranial skeleton shares many unique features with the shelled body plan of turtles2,3,4. Scepticism regarding the status ofEunotosaurus as the earliest stem turtle arises from the possibility that these shell-related features are the products of evolutionary convergence. Our phylogenetic analyses indicate strong cranial support forEunotosaurus as a critical transitional form in turtle evolution, thus fortifying a 40-million-year extension to the turtle stem and moving the ecological context of its origin back onto land8,9. Furthermore, we find unexpected evidence thatEunotosaurus is a diapsid reptile in the process of becoming secondarily anapsid. This is important because categorizing the skull based on the number of openings in the complex of dermal bone covering the adductor chamber has long held sway in amniote systematics10, and still represents a common organizational scheme for teaching the evolutionary history of the group. These discoveries allow us to articulate a detailed and testable hypothesis of fenestral closure along the turtle stem. Our results suggest thatEunotosaurus represents a crucially important link in a chain that will eventually lead to consilience in reptile systematics, paving the way for synthetic studies of amniote evolution and development.

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Figure 1: Competing hypotheses for the origin of the anapsid skull of modern turtles.
Figure 2: The adult skull of the early stem turtleEunotosaurus africanus.
Figure 3: The body plan of the early stem turtleEunotosaurusafricanus.
Figure 4: Generalized amniote phylogeny showing sequence of major transformations in the origin of the turtle skull.

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Acknowledgements

We thank J. Botha-Brink, E. Butler, S. Kaal, E. De Kock, J. Neveling and R. Smith for access toEunotosaurus specimens. M. Fox and Z. Erasmus prepared fossil material. M. Colbert, J. Maisano, M. Hill and J. Thostenson are acknowledged for their help with the digital data. We thank A. Balanoff, D. Dykes, J. Gauthier, R. Hill, B. Rubidge, R. Smith and K. de Queiroz for helpful discussions. G.S.B. extends special thanks to the Academic Technologies Group at NYIT for their support in the digital visualization of anatomical data.

Author information

Authors and Affiliations

  1. Department of Anatomy, New York Institute of Technology, College of Osteopathic Medicine, Old Westbury, 11568, New York, USA

    G. S. Bever

  2. Division of Paleontology, American Museum of Natural History, New York, 10024, New York, USA

    G. S. Bever

  3. Evolutionary Studies Institute, University of the Witwatersrand, Private Bag 3, P.O. WITS, Johannesburg, 2050, South Africa

    G. S. Bever & Tyler R. Lyson

  4. Department of Earth Sciences, Denver Museum of Nature and Science, Denver, 80205, Colorado, USA

    Tyler R. Lyson

  5. Department of Geology & Geophysics and Peabody Museum of Natural History, Yale University, New Haven, 06520, Connecticut, USA

    Daniel J. Field & Bhart-Anjan S. Bhullar

  6. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, 60637, Illinois, USA

    Bhart-Anjan S. Bhullar

Authors
  1. G. S. Bever

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  2. Tyler R. Lyson

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  3. Daniel J. Field

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  4. Bhart-Anjan S. Bhullar

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Contributions

G.S.B. designed the study, processed the CT data, performed the analytical work, constructed the figures, and wrote the paper. T.R.L. performed analytical work, assisted writing the paper, and assisted with figures. D.J.F. and B.-A.S.B. performed analytical work and assisted writing the paper.

Corresponding author

Correspondence toG. S. Bever.

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Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Digital reconstruction of segmented cranial elements ofEunotosaurus africanus CM 777.

a, Palatal view with the lower jaws digitally removed and major roofing elements not rendered.b, Anteromedial view of left palate showing moderately sized suborbital fenestra.c,d, Posteromedial (c) and anterolateral (d) views of left quadrate, prootic, stapes, epipterygoid and midline parabasisphenoid.e, Right lateral view of anterior braincase wall and surrounding elements. Note sutural contact of prootic and quadrate.f–k, Lower jaws in dorsal (f), ventral (g), left lateral (h), medial (left jaw) (i), anterior (j), and posterior (k) views. an, angular; ar, articular; bs, parabasisphenoid; co, coronoid; d, dentary; ect, ectopterygoid; epi, epipterygoid; fr, frontal; ju, jugal; la, lacrimal; ls, laterosphenoid; mx, maxilla; op, opisthotic; pa, parietal; pf, prefrontal; pl, palatine; pm, premaxilla; po, postorbital; pof, postfrontal; pr, prootic; pra, prearticular; pt, pterygoid; q, quadrate; qj, quadratojugal; s, stapes; sq, squamosal; sof, suborbital fenestra; sp., splenial; st, supratemporal; sa, surangular; v, vomer; II, inferred exit point for orbital nerve; V, prootic incisure, exit point for trigeminal nerve.

Extended Data Figure 2 The juvenile skull ofEunotosaurus africanus (SAM-PK-K7909) showing clear expression of both LTF and UTF.

a,b, Left lateral view with the rostrum held horizontally (a) and slightly downturned (b).c, Close-up view of fenestrated cheek in right lateral view. The size of the fenestrae decreases in the late stages of postnatal ontogeny through expansion of the surrounding dermal bones. The upper temporal fenestra is eventually obscured by the late-stage ontogenetic development of an elongate supratemporal.

Extended Data Figure 3 Digitally segmented and reconstructed cranial elements ofEunotosaurus africanus (CM86-341).

a–d, Right lateral view (a), anterior (b), posterior (c), and right medial (d) views. an, angular; d, dentary; epi, epipterygoid; ju, jugal; la, lacrimal; ‘ls’, ‘laterosphenoid’; mx, maxilla; pa, parietal; pf, prefrontal; pl, palatine; po, postorbital; pof, postfrontal; pt, pterygoid; q, quadrate; qj, quadratojugal; sa + ar, surangular and articular; sq, squamosal; st, supratemporal; UTF, upper temporal fenestra; ?, unclear identity.

Extended Data Figure 4 Strict consensus of two most parsimonious recovered from total character matrix.

Bremer support values are provided for each clade (above line). Bootstrap values exceeding 50% are provided (below line). AEunotosaurus–turtle clade is extremely well supported. That this pan-turtle lineage originated somewhere within the radiation of anatomically diapsid reptiles is well supported, although a refined phylogenetic position remains morphologically elusive. Tree length = 1,087; consistency index = 0.4013; retention index = 0.590.

Extended Data Figure 5 Bayesian tree topology derived from total matrix (50% majority rule consensus).

An exclusiveEunotosaurus–turtle clade is recovered with 100% posterior probability. This pan-turtle lineage is nested within the radiation of anatomically diapsid reptiles; however, in contrast to the parsimony solution, turtles are excluded from crown-group Diapsida. The Bayesian results agree with the parsimony in revealing strong support that: (1)Eunotosaurus is an early stem-group turtle; and (2) the ancestral stem turtle expressed a fully diapsid skull. The two analyses also agree that there is currently poor morphological support for a refined position of turtles within the greater diapsid radiation.

Extended Data Figure 6 Strict consensus of 13 most parsimonious trees recovered from cranial-only matrix.

TheEunotosaurus–turtle clade is recovered, which supports the hypothesis that the postcranial synapomorphies ofEunotosaurus and turtles are homologous and not the products of convergence. Tree length = 777; consistency index = 0.3956; retention index = 0.4743.

Extended Data Figure 7 Bayesian tree topology derived from cranial-only matrix (50% majority rule consensus).

When studied in isolation, cranial anatomy provides poor resolution of the deep divergences within Pan-Reptilia, but aEunotosaurus–turtle signal is clearly present.

Supplementary information

Supplementary Information

This file contains a Supplementary Discussion, Supplementary References and Supplementary Tables 1-4. (PDF 1311 kb)

Supplementary Data

This file contains the data matrix used in phylogenetic analyses. (TXT 14 kb)

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Bever, G., Lyson, T., Field, D.et al. Evolutionary origin of the turtle skull.Nature525, 239–242 (2015). https://doi.org/10.1038/nature14900

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Editorial Summary

Eunotosaurus was turning turtle

The evolution of the early reptiles is a complicated story and one particular event — the inferred transformation between an ancestral turtle with a diapsid skull (with openings in the skull behind each eye) to the closed, anapsid condition of modern turtles — has remained elusive in the fossil record.Eunotosaurus africanus is an unusual reptile that lived 260 million years ago in what is now South Africa. Its oddities include flared and expanded ribs, which some have suggested represent the early stirrings of testudinates (turtles and tortoises). Computed tomography and phylogenetic analysis of theE. africanus skull now suggests that not only isEunotosaurus an early relative of the group, but that it is a diapsid caught in the act of evolving towards a secondarily anapsid state.

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