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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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References

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

    Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Domyan, E. T. & Shapiro, M. D. Pigeonetics takes flight: evolution, development, and genetics of intraspecific variation. Dev. Biol. http://dx.doi.org/10.1016/j.ydbio.2016.11.008 (in the press).

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  10. Wagner G. P. & Altenberg, L. Complex adaptations and the evolution of evolvability. Evolution 50, 967–976 (1996).

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  12. Wagner, G. P., Pavlicev, M. & Cheverud, J. The road to modularity. Nat. Rev. Genet. 8, 921–931 (2007).

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  14. Baptista, L. F., Gomez Martinez, J. E. & Horblit, H. M. Darwin’s pigeons and the evolution of the columbiforms: recapitulation of ancient genes. Acta Zool. Mex. 25, 719–741 (2009).

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  20. Linde-Medina, M. & Newman, S. A. Limb, tooth, beak: three modes of development and evolutionary innovation of form. J. Bioscience 39, 211–223 (2014).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  23. Drake, A. G. & Klingenberg, C. P. Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am. Nat. 175, 289–301 (2010).

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Marcucio, R. S., Young, N. M., Hu, D. & Hallgrímsson, B. Mechanisms that underlie co-variation of the brain and face. Genesis 49, 177–189 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  30. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2016); https://www.R-project.org

  31. Marroig, G. & Cheverud, J. M. 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).

    Article  CAS  PubMed  Google Scholar 

  32. Wagner, G. P. 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).

    Article  Google Scholar 

  33. Pavlicev, M., Cheverud, J. M. & Wagner, G. P. Measuring morphological integration using eigenvalue variance. Evol. Biol. 36, 157–170 (2009).

    Article  Google Scholar 

  34. Young, N. M., Wagner, G. P. & Hallgrímsson, B. Development and the evolvability of human limbs. Proc. Natl Acad. Sci. USA 107, 3400–3405 (2010).

    Article  CAS  PubMed  Google Scholar 

  35. Zelditch, M. L., Swiderski, D. L. & Sheets, H. D. Geometric Morphometrics for Biologists: A Primer (Academic, 2012).

    Google Scholar 

  36. Nealen, P. M. & Ricklefs, R. Early diversification of the avian brain:body relationship. J. Zool. 253, 391–404 (2001).

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  39. Adams, D. C. & Otarola-Castillo, E. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  42. Maddison, W. P. & Maddison, D. R. Mesquite: A Modular System for Evolutionary Analysis Version 3.10 (accessed 7 January 2016); http://mesquiteproject.org

  43. Klingenberg, C. P. & Gidaszewski, N. A. Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Syst. Biol. 59, 245–261 (2010).

    Article  CAS  PubMed  Google Scholar 

  44. Blomberg, S. P., Garland, T. & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

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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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