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Dinosaur ossification centres in embryonic birds uncover developmental evolution of the skull

Nature Ecology & Evolution volume 2, pages 1966–1973 (2018)Cite this article

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Abstract

Radical transformation of the skull characterizes bird evolution. An increase in the relative size of the brain and eyes was presumably related to the loss of two bones surrounding the eye, the prefrontal and postorbital. We report that ossification centres of the prefrontal and postorbital are still formed in bird embryos, which then fuse seamlessly to the developing nasal and frontal bones, respectively, becoming undetectable in the adult. The presence of a dinosaur-like ossification pattern in bird embryos is more than a trace of their evolutionary past: we show how persistent modularity of ossification centres has allowed for evolutionary re-organization of skull architecture in evolution. Our findings also demonstrate that enigmatic mesodermal cells forming the posterior region of the avian frontal correspond to the ossification centre of the postorbital, not the parietal, and link its failure to develop into an adult bone to its incorporation into the expanded braincase of birds.

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Fig. 1: Early formation of a prefrontal ossification centre in a palaeognathous bird.
Fig. 2: Early formation of a postorbital ossification centre in neognathous birds.
Fig. 3: Evolution of adult circumorbital bones along the dinosaur–bird transition.
Fig. 4: Formation of the prefrontal as a separate ossification centre in fossil Paraves.
Fig. 5: Evolutionary consequences of embryonic modularity.

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High-resolution photographs of the specimens are available in the figures and also can be provided by request.

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Acknowledgements

We wish to thank B.-A. Bhullar for kindly allowing us to examine and photograph embryos of A. mississippiensis. Special thanks go to M. Sallaberry and J. Mpodozis at Universidad de Chile. This work was funded by grants Anillo ACT172099 and Fondecyt 1150906 (Conicyt, Government of Chile) to A.O.V. This work is dedicated to the memory of Professor Juan Fernández Hidalgo.

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Author notes

  1. Daniel Smith-Paredes

    Present address: Department of Geology and Geophysics, Yale University, New Haven, CT, USA

  2. Daniel Núñez-León

    Present address: Paläontologisches Institut und Museum, Universität Zürich, Zürich, Switzerland

Authors and Affiliations

  1. Laboratorio de Ontogenia y Filogenia, Departamento de Biología, Facultad de Ciencias de la Universidad de Chile, Santiago, Chile

    Daniel Smith-Paredes, Daniel Núñez-León, Sergio Soto-Acuña, João Francisco Botelho & Alexander O. Vargas

  2. Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China

    Jingmai O’Connor

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Contributions

D.S.-P. and A.O.V. conceived and planned the research. D.S.-P. and D.N.-L. collected, cleared and stained embryos and analysed embryological data. D.S.-P., S.S.-A. and J.O. analysed fossil specimens and palaeontological data. D.S.-P., D.N.-L., S.S.-A., J.O., J.F.B. and A.O.V contributed to the writing of the paper.

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Correspondence to Daniel Smith-Paredes or Alexander O. Vargas.

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Smith-Paredes, D., Núñez-León, D., Soto-Acuña, S. et al. Dinosaur ossification centres in embryonic birds uncover developmental evolution of the skull. Nat Ecol Evol 2, 1966–1973 (2018). https://doi.org/10.1038/s41559-018-0713-1

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