Craniofacial diversification in the domestic pigeon and the evolution of the avian skull

Abstract

A central question in evolutionary developmental biology is how highly conserved developmental systems can generate the remarkable phenotypic diversity observed among distantly related species. In part, this paradox reflects our limited knowledge about the potential for species to both respond to selection and generate novel variation. Consequently, the developmental links between small-scale microevolutionary variations within populations to larger macroevolutionary patterns among species remain unbridged. Domesticated species, such as the pigeon, are unique resources for addressing this question, because a history of strong artificial selection has significantly increased morphological diversity, offering a direct comparison of the developmental potential of a single species to broader evolutionary patterns. Here, we demonstrate that patterns of variation and covariation within and between the face and braincase in domesticated breeds of the pigeon are predictive of avian cranial evolution. These results indicate that selection on variation generated by a conserved developmental system is sufficient to explain the evolution of crania as different in shape as the albatross or eagle, parakeet or hummingbird. These ‘rules’ of cranio­facial variation are a common pattern in the evolution of a broad diversity of vertebrate species and may ultimately reflect structural limitations of a shared embryonic bauplan on functional variation.

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Figure 1: Variation in the pigeon craniofacial skeleton compared with avian diversity.
Figure 2: Results of the PCA from linear distance data.
Figure 3: Pigeon craniofacial shape morphospace.
Figure 4: Results of the PLS analysis of face and braincase modules.
Figure 5: Comparison of craniofacial diversification in domesticated pigeon breeds with the avian radiation.

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Acknowledgements

We thank J. DeCarlo for kindly donating specimens of domestic pigeon breeds, A. Goode for preparing their skeletons and R. Johnston for generously sharing his original pigeon data. Non-pigeon avian CT data were provided courtesy of the University of Texas High Resolution X-ray CT Facility (UTCT) (National Science Foundation grant number IIS-0208675). Research reported in this publication was supported by the National Institute of Dental and Craniofacial Research of the National Institutes of Health under Award Numbers F32DE018596 (to N.M.Y.), R01DE019638 (to R.S.M. and B.H.) and R01DE021708 (to R.S.M. and B.H.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Contributions

N.M.Y. designed the research. N.M.Y. and J.W.F. collected pigeon specimens. N.M.Y. and M.L.-M. performed the analyses. N.M.Y., M.L.-M., B.H., and R.S.M. contributed to the interpretation of the results. N.M.Y. drafted the paper. All authors contributed to the final version of the paper.

Corresponding author

Correspondence to Nathan M. Young.

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The authors declare no competing financial interests.

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Supplementary Tables 1–7, Supplementary Figures 1–10. (PDF 2647 kb)

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Young, N., Linde-Medina, M., Fondon, J. et al. Craniofacial diversification in the domestic pigeon and the evolution of the avian skull. Nat Ecol Evol 1, 0095 (2017). https://doi.org/10.1038/s41559-017-0095

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