Article

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

  • Nature Ecology & Evolution 1, Article number: 0095 (2017)
  • doi:10.1038/s41559-017-0095
  • Download Citation
Received:
Accepted:
Published online:

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.

  • Subscribe to Nature Ecology & Evolution for full access:

    $99

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    The Variation of Animals and Plants under Domestication Vol. 1 (John Murray, 1868).

  2. 2.

    On the Origin of Species by Means of Natural Selection (John Murray, 1859).

  3. 3.

    et al. Divergence, convergence, and the ancestry of feral populations in the domestic rock pigeon. Curr. Biol. 22, 302–308 (2012).

  4. 4.

    Genomic diversity and evolution of the head crest in the rock pigeon. Science 339, 1063–1067 (2013).

  5. 5.

    & Pigeonetics takes flight: evolution, development, and genetics of intraspecific variation. Dev. Biol. (in the press).

  6. 6.

    Genic and organismic selection. Evolution 34, 825–843 (1980).

  7. 7.

    Phenotypic, genetic, and environmental integration in the cranium. Evolution 36, 499–516 (1982).

  8. 8.

    et al. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol. Biol. 36, 355–376 (2009).

  9. 9.

    Developmental integration and the evolution of pleiotropy. Am. Zool. 36, 44–50 (1996).

  10. 10.

    & Complex adaptations and the evolution of evolvability. Evolution 50, 967–976 (1996).

  11. 11.

    et al. Developmental constraints and evolution. Q. Rev. Biol. 60, 265–287 (1985).

  12. 12.

    , & The road to modularity. Nat. Rev. Genet. 8, 921–931 (2007).

  13. 13.

    Evolution in the rock dove: skeletal morphology. Auk 109, 530–542 (1992).

  14. 14.

    , & Darwin’s pigeons and the evolution of the columbiforms: recapitulation of ancient genes. Acta Zool. Mex. 25, 719–741 (2009).

  15. 15.

    et al. Bmp4 and morphological variation of beaks in Darwin’s finches. Science 305, 1462–1465 (2004).

  16. 16.

    et al. Molecular shaping of the beak. Science 305, 1465–1466 (2004).

  17. 17.

    et al. The calmodulin pathway and evolution of elongated beak morphology in Darwin’s finches. Nature 442, 563–567 (2006).

  18. 18.

    et al. Morphoregulation of avian beaks: comparative mapping of growth zone activities and morphological evolution. Dev. Dynam. 235, 1400–1412 (2006).

  19. 19.

    et al. Shared developmental programme strongly constrains beak shape diversity in songbirds. Nat. Commun. 5, 3700 (2015).

  20. 20.

    & Limb, tooth, beak: three modes of development and evolutionary innovation of form. J. Bioscience 39, 211–223 (2014).

  21. 21.

    et al. Two developmental modules establish 3D beak-shape variation in Darwin’s finches. Proc. Natl Acad. Sci. USA 108, 4057–4062 (2011).

  22. 22.

    et al. The shapes of bird beaks are highly controlled by nondietary factors. Proc. Natl Acad. Sci. USA 113, 5352–5357 (2016).

  23. 23.

    & Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am. Nat. 175, 289–301 (2010).

  24. 24.

    et al. Pervasive genetic integration directs the evolution of human skull shape. Evolution 66, 1010–1023 (2010).

  25. 25.

    et al. Facial surface morphology predicts variation in internal skeletal shape. Am. J. Orthod. Dent. Orthop. 149, 501–508 (2016).

  26. 26.

    et al. The evolution of modularity in the mammalian skull I: Morphological integration patterns and magnitudes. Evol. Biol. 36, 118–135 (2009).

  27. 27.

    et al. Embryonic bauplans and the developmental origins of facial diversity and constraint. Development 141, 1059–1063 (2014).

  28. 28.

    , , & Mechanisms that underlie co-variation of the brain and face. Genesis 49, 177–189 (2011).

  29. 29.

    et al. smatr 3—an R package for estimation and inference about allometric lines. Methods Ecol. Evol. 3, 257–259 (2012).

  30. 30.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016);

  31. 31.

    & A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys. Evolution 55, 2576–2600 (2001).

  32. 32.

    On the eigenvalue distribution of genetic and phenotypic dispersion matrices: Evidence for a non-random origin of quantitative genetic variation. J. Math. Biol. 21, 77–95 (1984).

  33. 33.

    , & Measuring morphological integration using eigenvalue variance. Evol. Biol. 36, 157–170 (2009).

  34. 34.

    , & Development and the evolvability of human limbs. Proc. Natl Acad. Sci. USA 107, 3400–3405 (2010).

  35. 35.

    , & Geometric Morphometrics for Biologists: A Primer (Academic, 2012).

  36. 36.

    & Early diversification of the avian brain:body relationship. J. Zool. 253, 391–404 (2001).

  37. 37.

    Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Evol. Dev. 11, 405–421 (2009).

  38. 38.

    Evaluating modularity in morphometric data: challenges with the RV coefficient and a new test measure. Methods Ecol. Evol. 7, 565–572 (2016).

  39. 39.

    & geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).

  40. 40.

    Integration, disintegration, and self-similarity: characterizing the scales of shape variation in landmark data. Evol. Biol. 42, 395–426 (2015).

  41. 41.

    et al. The global diversity of birds in space and time. Nature 491, 444–448 (2012).

  42. 42.

    & Mesquite: A Modular System for Evolutionary Analysis Version 3.10 (accessed 7 January 2016);

  43. 43.

    & Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Syst. Biol. 59, 245–261 (2010).

  44. 44.

    , & Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003).

  45. 45.

    A generalized Κ statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst. Biol. 63, 685–697 (2014).

  46. 46.

    & Convergence and divergence in the evolution of cat skulls: Temporal and spatial patterns of morphological diversity. PLoS ONE 7, e39752 (2012).

  47. 47.

    MorphoJ: an integrated software package for geometric morphometrics. Mol. Ecol. Resour. 11, 353–357 (2011).

Download references

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.

Author information

Affiliations

  1. University of California San Francisco, Department of Orthopaedic Surgery, 2550 23rd Street, San Francisco, California 94115, USA

    • Nathan M. Young
    • , Marta Linde-Medina
    •  & Ralph S. Marcucio
  2. University of Texas at Arlington, Department of Biological Sciences, Texas 76019, USA

    • John W. Fondon
  3. University of Calgary, Department of Cell Biology and Anatomy and the Alberta Children’s Hospital Research Institute, Alberta T2N 4N1, Canada

    • Benedikt Hallgrímsson

Authors

  1. Search for Nathan M. Young in:

  2. Search for Marta Linde-Medina in:

  3. Search for John W. Fondon in:

  4. Search for Benedikt Hallgrímsson in:

  5. Search for Ralph S. Marcucio in:

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Nathan M. Young.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Tables 1–7, Supplementary Figures 1–10.