Article

The skull roof tracks the brain during the evolution and development of reptiles including birds

  • Nature Ecology & Evolution 115431550 (2017)
  • doi:10.1038/s41559-017-0288-2
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Abstract

Major transformations in brain size and proportions, such as the enlargement of the brain during the evolution of birds, are accompanied by profound modifications to the skull roof. However, the hypothesis of concerted evolution of shape between brain and skull roof over major phylogenetic transitions, and in particular of an ontogenetic relationship between specific regions of the brain and the skull roof, has never been formally tested. We performed 3D morphometric analyses to examine the deep history of brain and skull-roof morphology in Reptilia, focusing on changes during the well-documented transition from early reptiles through archosauromorphs, including nonavian dinosaurs, to birds. Non-avialan taxa cluster tightly together in morphospace, whereas Archaeopteryx and crown birds occupy a separate region. There is a one-to-one correspondence between the forebrain and frontal bone and the midbrain and parietal bone. Furthermore, the position of the forebrain–midbrain boundary correlates significantly with the position of the frontoparietal suture across the phylogenetic breadth of Reptilia and during the ontogeny of individual taxa. Conservation of position and identity in the skull roof is apparent, and there is no support for previous hypotheses that the avian parietal is a transformed postparietal. The correlation and apparent developmental link between regions of the brain and bony skull elements are likely to be ancestral to Tetrapoda and may be fundamental to all of Osteichthyes, coeval with the origin of the dermatocranium.

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Acknowledgements

We are grateful to E. J. Rayfield, A. R. Cuff, Y. Kobayashi, S. Chatterjee, A. Turner and L. Witmer for providing CT data; to G. Watkins-Colwell for assisting with cleared and stained squamate embryo specimens; and to D. Smith for imaging. F. A. Jenkins, Jr, J. A. Gauthier, G. Wagner and G. Navalon provided useful discussion. E. M. Sefton, H. Maddin and J. Hanken commented on the early stages of the work as it was underway. All Yale authors are supported by funds from Yale University. D.J.F. is supported in part by NSF DDIG DEB 1500798 to B.-A.S.B and D.J.F. A.P. is supported by an NSF Postdoctoral Research Fellowship in Biology. J.C. was partially funded by an NSF Graduate Research Fellowship and by NSF DDIG DEB 1501690. A.A. was supported by NSF grant 1257122, the Templeton Foundation grant RFP-12-0 and by funds from Imperial College London. G.S.B, A.M.B., and M.A.N. are supported in part by NSF DEB 1457181.

Author information

Author notes

    • Eva Hoffman

    Present address: Jackson School of Geosciences and Vertebrate Paleontology Laboratory, The University of Texas at Austin, Austin, TX, 78705, USA

Affiliations

  1. Department of Geology and Geophysics and Peabody Museum of Natural History, Yale University, New Haven, CT, 06520, USA

    • Matteo Fabbri
    • , Nicolás Mongiardino Koch
    • , Adam C. Pritchard
    • , Michael Hanson
    • , Eva Hoffman
    • , Daniel J. Field
    •  & Bhart-Anjan S. Bhullar
  2. Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA

    • Gabriel S. Bever
    •  & Amy M. Balanoff
  3. Department of Organismal and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, Cambridge, MA, 02138, USA

    • Zachary S. Morris
    •  & Jasmin Camacho
  4. Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath, BA2 7AY, UK

    • Daniel J. Field
  5. Macaulay Curator, Division of Paleontology, American Museum of Natural History, New York, NY, 10024, USA

    • Mark A. Norell
  6. Natural History Department, Iziko South African Museum, Cape Town, 8000, South Africa

    • Roger M. Smith
  7. Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot, Berkshire, SL5 7PY, UK

    • Arhat Abzhanov
  8. Natural History Museum, London, SW7 5BD, UK

    • Arhat Abzhanov

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Contributions

B-A.S.B. and A.A. conceived and planned the research. M.F., A.C.P., M.H., E.H., G.S.B., A.M.B., J.C., Z.M., D.J.F. and B.-A.S.B. scanned specimens and performed segmentation. M.F., N.M.K., A.C.P., M.H., and B.-A.S.B. placed landmarks and performed morphometric analyses. M.F. and N.M.K. performed correlation tests. M.F., N.M.K., A.C.P., M.H., E.H., G.S.B., T.B.R., A.A., and B.-A.S.B., wrote the paper. M.A.N. and R.M.S. provided CT data and assisted in anatomical interpretation.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Matteo Fabbri or Arhat Abzhanov or Bhart-Anjan S. Bhullar.

Electronic supplementary material

  1. Supplementary Information

    Supplementary Figures 1–5, Supplementary Tables 1–3

  2. Supplementary Data 1

    Landmark data for geometric morphometrics