Birds have paedomorphic dinosaur skulls

Journal name:
Nature
Volume:
487,
Pages:
223–226
Date published:
DOI:
doi:10.1038/nature11146
Received
Accepted
Published online

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.

At a glance

Figures

  1. Archosaur phylogeny and ontogeny.
    Figure 1: Archosaur phylogeny and ontogeny.

    a, Phylogeny of included taxa. Sources are listed in Supplementary Information. Colours serve as keys to data points in Figs 2 and 5. Heterochronic transformations discussed in the text are enumerated as Roman numerals. bd, skulls of selected archosaurs: Alligator 46-day embryo (b, left) and adult (b, right); Coelophysis (primitive dinosaur) juvenile (c, left) and adult (c, right); Archaeopteryx (stem-group bird) juvenile (d, left) and adult (d, right).

  2. PCA plot with outline images of hypothetical extremes along each axis, set on deformation grids from average.
    Figure 2: PCA plot with outline images of hypothetical extremes along each axis, set on deformation grids from average.

    Colours correspond to those in Fig. 1a. Arrows indicate ontogenies. Major groupings are outlined, shaded and labelled. Group A are non-eumaniraptoran and secondarily large-bodied eumaniraptoran theropod adults; group B are adults of basal eumaniraptorans and early avialans, and embryos and perinates of other archosaurs; group C are crown-group bird embryos, juveniles and adults.

  3. Summary of ontogenetic changes in archosaur skulls; outlines on deformation grids from average.
    Figure 3: Summary of ontogenetic changes in archosaur skulls; outlines on deformation grids from average.

    a, Alligator. b, Compsognathidae. c, Therizinosauridae. d, Archaeopteryx. e, Enantiornithes. f, Confuciusornis. g, Ostriches (Struthio).

  4. Similarity of embryonic Alligator and adult Confuciusornis skulls.
    Figure 4: Similarity of embryonic Alligator and adult Confuciusornis skulls.

    Superimposition of Alligator embryo skull (green) onto Alligator adult skull (red, left) and onto Confuciusornis adult skull (red, right), showing the nearly identical skull configuration of the latter two and indicating paedomorphic cranial morphology in Confuciusornis.

  5. Summary of heterochrony and phylogeny in bird skull evolution.
    Figure 5: Summary of heterochrony and phylogeny in bird skull evolution.

    A phylogenetic sequence with skull outlines set on deformation grids is depicted from the primitive stem-group archosaur Euparkeria to the modern emu Dromaius. Heterochronic transformations referred to in the text are enumerated with Roman numerals. Major anatomical regions involved in heterochronic transformations are labelled.

  6. Regression of centroid size (as an indicator of skull size) on shape change, and distribution of vector angles.
    Figure 6: Regression of centroid size (as an indicator of skull size) on shape change, and distribution of vector angles.

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Author information

Affiliations

  1. Department of Organismic and Evolutionary Biology, Harvard University, 16Divinity 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, 1University 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

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.

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The authors declare no competing financial interests.

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Supplementary information

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  1. Supplementary Information (3.1M)

    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. Supplementary Animation (2.3M)

    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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