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Birds have paedomorphic dinosaur skulls

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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Figure 1: Archosaur phylogeny and ontogeny.
Figure 2: PCA plot with outline images of hypothetical extremes along each axis, set on deformation grids from average.
Figure 3: Summary of ontogenetic changes in archosaur skulls; outlines on deformation grids from average.
Figure 4: Similarity of embryonic Alligator and adult Confuciusornis skulls.
Figure 5: Summary of heterochrony and phylogeny in bird skull evolution.
Figure 6

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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.

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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.

Corresponding authors

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

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The authors declare no competing financial interests.

Supplementary information

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). (PDF 3234 kb)

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. (ZIP 2360 kb)

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Bhullar, BA., Marugán-Lobón, J., Racimo, F. et al. Birds have paedomorphic dinosaur skulls. Nature 487, 223–226 (2012). https://doi.org/10.1038/nature11146

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