Letter | Published:

Birds have paedomorphic dinosaur skulls

Nature volume 487, pages 223226 (12 July 2012) | Download Citation

Abstract

The interplay of evolution and development has been at the heart of evolutionary theory for more than a century1. Heterochrony—change in the timing or rate of developmental events—has been implicated in the evolution of major vertebrate lineages such as mammals2, including humans1. Birds are the most speciose land vertebrates, with more than 10,000 living species3 representing a bewildering array of ecologies. Their anatomy is radically different from that of other vertebrates. The unique bird skull houses two highly specialized systems: the sophisticated visual and neuromuscular coordination system4,5 allows flight coordination and exploitation of diverse visual landscapes, and the astonishing variations of the beak enable a wide range of avian lifestyles. Here we use a geometric morphometric approach integrating developmental, neontological and palaeontological data to show that the heterochronic process of paedomorphosis, by which descendants resemble the juveniles of their ancestors, is responsible for several major evolutionary transitions in the origin of birds. We analysed the variability of a series of landmarks on all known theropod dinosaur skull ontogenies as well as outgroups and birds. The first dimension of variability captured ontogeny, indicating a conserved ontogenetic trajectory. The second dimension accounted for phylogenetic change towards more bird-like dinosaurs. Basally branching eumaniraptorans and avialans clustered with embryos of other archosaurs, indicating paedomorphosis. Our results reveal at least four paedomorphic episodes in the history of birds combined with localized peramorphosis (development beyond the adult state of ancestors) in the beak. Paedomorphic enlargement of the eyes and associated brain regions parallels the enlargement of the nasal cavity and olfactory brain in mammals6. This study can be a model for investigations of heterochrony in evolutionary transitions, illuminating the origin of adaptive features and inspiring studies of developmental mechanisms.

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Acknowledgements

We thank R. M. Elsey and colleagues at the Rockefeller Wildlife Refuge, Louisiana Department of Wildlife and Fisheries for assistance in obtaining alligator embryos, S. Majadla for imaging assistance, C. Sánchez for constructing the Supplementary Movie, I. Sarris for assistance with the R script packages, and J. B. Losos, H. E. Hoekstra, F. A. Jenkins Jr and B. Zweig for comments that improved the manuscript. B.-A.S.B. was partly funded by National Science Foundation dissertation improvement grant 1110564. J.M.-L. was supported by project BFU2008-00642.

Author information

Affiliations

  1. Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA

    • Bhart-Anjan S. Bhullar
    • , Fernando Racimo
    •  & Arhat Abzhanov
  2. Unidad de Paleontología, Departamento de Biología, Universidad Autónoma de Madrid, 28049 Cantoblanco (Madrid), Spain

    • Jesús Marugán-Lobón
  3. Department of Anatomy, New York College of Osteopathic Medicine of New York Institute of Technology, Old Westbury, New York 11568-8000, USA

    • Gabe S. Bever
  4. Department of Geological Sciences, Jackson School of Geosciences, The University of Texas at Austin, 1 University Station C1100, Austin, Texas 78712, USA

    • Timothy B. Rowe
  5. Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024-5192, USA

    • Mark A. Norell

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Contributions

B.-A.S.B. and A.A. designed the study. B.-A.S.B. wrote the paper and performed CT scans, data entry and analytical work. J.M.-L. performed analytical work and assisted with writing and figures. F.R. performed data entry and analytical work. G.B. helped conceive the project and performed data processing on new CT data. T.B.R. contributed CT data and assisted in data interpretation and writing the paper. M.A.N. contributed the major hypotheses to be tested, provided CT data and assisted in writing the paper. A.A. co-wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

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

Supplementary information

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  1. 1.

    Supplementary Information

    This file contains Supplementary Data 1-13, which comprises: Supplementary Text (1-9) and (11); Supplementary Figures 1-10 (10); Supplementary Methods and Supplementary Tables 1-4 (12); and Supplementary References (13) = – see Contents for details. Page 2 contains instructions for the Supplementary Animation files (see separate zipped files).

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  1. 1.

    Supplementary Animation

    This zipped file contains a flash animation file (.swf) and a zipped file, which contains the ‘ontology.htm’ and ‘ontology.swf’ files. Instructions on how to open these files is given on page 2 of the Supplementary Information file.

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DOI

https://doi.org/10.1038/nature11146

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