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Research Article

The shapes of bird beaks are highly controlled by nondietary factors

Jen A. Bright, Jesús Marugán-Lobón, Samuel N. Cobb, and View ORCID ProfileEmily J. Rayfield
PNAS first published April 28, 2016; https://doi.org/10.1073/pnas.1602683113
Jen A. Bright
aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
bDepartment of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom;
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  • For correspondence: jen.bright@gmail.com
Jesús Marugán-Lobón
cUnidad de Paleontología, Departamento de Biología, Universidad Autónoma de Madrid, Cantoblanco, Madrid 28049, Spain;
dDinosaur Institute, Natural History Museum of Los Angeles County, Los Angeles, CA 90007;
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Samuel N. Cobb
eDepartment of Archaeology, University of York, York YO10 5DD, United Kingdom;
fHull York Medical School, University of York, York YO10 5DD, United Kingdom
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Emily J. Rayfield
aSchool of Earth Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
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  • ORCID record for Emily J. Rayfield
  1. Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved March 30, 2016 (received for review February 19, 2016)

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Significance

We show that beak and skull shapes in birds of prey (“raptors”) are strongly coupled and largely controlled by size. This relationship means that, rather than being able to respond independently to natural selection, beak shapes are highly constrained to evolve in a particular way. The main aspects of shape variation seem to correspond with specific genes active during development. Because raptors are not each other’s closest relatives, similar shape constraints may therefore have been present in the ancestors of all modern songbirds, including Darwin’s finches, the classic example of explosive evolution in birds. If this hypothesis is true, then such classic examples may be unusual, needing first to break a genetic lock before their beaks could evolve new shapes.

Abstract

Bird beaks are textbook examples of ecological adaptation to diet, but their shapes are also controlled by genetic and developmental histories. To test the effects of these factors on the avian craniofacial skeleton, we conducted morphometric analyses on raptors, a polyphyletic group at the base of the landbird radiation. Despite common perception, we find that the beak is not an independently targeted module for selection. Instead, the beak and skull are highly integrated structures strongly regulated by size, with axes of shape change linked to the actions of recently identified regulatory genes. Together, size and integration account for almost 80% of the shape variation seen between different species to the exclusion of morphological dietary adaptation. Instead, birds of prey use size as a mechanism to modify their feeding ecology. The extent to which shape variation is confined to a few major axes may provide an advantage in that it facilitates rapid morphological evolution via changes in body size, but may also make raptors especially vulnerable when selection pressures act against these axes. The phylogenetic position of raptors suggests that this constraint is prevalent in all landbirds and that breaking the developmental correspondence between beak and braincase may be the key novelty in classic passerine adaptive radiations.

  • geometric morphometrics
  • integration
  • allometry
  • birds
  • modularity

Footnotes

  • ↵1To whom correspondence should be addressed. Email: jen.bright{at}gmail.com.
  • Author contributions: J.A.B., J.M.-L., S.N.C., and E.J.R. designed research; J.A.B. performed research; J.A.B. and J.M.-L. analyzed data; and J.A.B., J.M.-L., S.N.C., and E.J.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1602683113/-/DCSupplemental.

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Bird beaks controlled by nondietary factors
Jen A. Bright, Jesús Marugán-Lobón, Samuel N. Cobb, Emily J. Rayfield
Proceedings of the National Academy of Sciences Apr 2016, 201602683; DOI: 10.1073/pnas.1602683113

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Bird beaks controlled by nondietary factors
Jen A. Bright, Jesús Marugán-Lobón, Samuel N. Cobb, Emily J. Rayfield
Proceedings of the National Academy of Sciences Apr 2016, 201602683; DOI: 10.1073/pnas.1602683113
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