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Patterns of skeletal integration in birds reveal that adaptation of element shapes enables coordinated evolution between anatomical modules

Nature Ecology & Evolution volume 5, pages 1250–1258 (2021)Cite this article

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Abstract

Birds show tremendous ecological disparity in spite of strong biomechanical constraints imposed by flight. Modular skeletal evolution is generally accepted to have facilitated this, with distinct body regions showing semi-independent evolutionary trajectories. However, this hypothesis has received little scrutiny. We analyse evolutionary modularity and ecomorphology using three-dimensional data from across the entire skeleton in a phylogenetically broad sample of extant birds. We find strongly modular evolution of skeletal element sizes within body regions (head, trunk, forelimb and hindlimb). However, element shapes show substantially less modularity, have stronger relationships to ecology, and provide evidence that ecological adaptation involves coordinated evolution of elements across different body regions. This complicates the straightforward paradigm in which modular evolution facilitated the ecological diversification of birds. Our findings suggest the potential for undetected patterns of morphological evolution in even well-studied groups, and advance the understanding of the interface between evolutionary integration and ecomorphology.

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Fig. 1: Landmarking scheme.
Fig. 2: Patterns of evolutionary integration across the bird skeleton.
Fig. 3: Patterns of evolutionary integration in taxonomic subsets.
Fig. 4: Illustrative figure.
Fig. 5: Ecomorphological relationships.

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Data availability

The specimen sources, scan parameters and metadata are reported in the Supplementary Information. All scans and 3D objects are available at www.morphosource.org/projects/00000C420, and the dataset is described in Bjarnason and Benson47.

Code availability

R version 3.63 was employed to run the analyses. The packages and functions used are described in detail in the Methods with citations. The codes written by assembling these pre-built functions are available upon request.

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Acknowledgements

For access to specimens, we thank J. White and J. Cooper (NHMUK), J. Hinshaw (UMMZ), M. Lowe and M. Brooke (UMZC), M. Carnall and E. Westwig (OUMNH), K. Zyskowski (YPM), and B. Marks and J. Bates (FMNH). For access to CT scanning facilities, we thank K. Smithson (Cambridge Biotomography Centre); T. Davies, B. Moon and L. Martin-Silverstone (University of Bristol); V. Fernandez (Natural History Museum); A. Neander and Z.-X. Luo (University of Chicago PaleoCT); and M. Friedman (University of Michigan). We thank E. Griffiths, S. Wright, S. Poindexter, A. Wolniewicz and S. Evers for segmenting digital bone models from the CT scan data. We acknowledge G. Navalón for reviewing our manuscript and making key suggestions concerning the presentation of our figures. Funding statement: This work was funded by the European Union’s Horizon 2020 research and innovation programme 2014–2018 under grant agreement no. 677774 (European Research Council Starting Grant: TEMPO). Grant no. 677774 applies to the work of R.B.J.B. and A.B.

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Author notes

  1. These authors contributed equally: Andrew Orkney, Alex Bjarnason.

Authors and Affiliations

  1. Department of Earth Sciences, University of Oxford, Oxford, UK

    Andrew Orkney, Alex Bjarnason, Brigit C. Tronrud & Roger B. J. Benson

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  1. Andrew Orkney
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Contributions

A.O. contributed to the analytical design, performed the analyses, drafted the manuscript, assembled co-author inputs to the final paper, and constructed and illustrated the figures. A.B. collected the landmark data and helped draft the analytical design. B.C.T. assembled the foot-use data. R.B.J.B. conceived and designed the analysis (with A.O.), collected the CT scan data, oversaw the collection of landmarks (with A.B.) and foot-use data (with B.C.T.), and provided key academic insight. All authors read, contributed to and approved the final manuscript.

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Correspondence to Andrew Orkney.

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The authors declare no competing interests.

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Peer review information Nature Ecology & Evolution thanks T. Alexander Dececchi and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Supplementary information

Supplementary Information

Supplementary foot-use ecological character descriptions, Figs. 1–34 and Tables 1 and 2.

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Orkney, A., Bjarnason, A., Tronrud, B.C. et al. Patterns of skeletal integration in birds reveal that adaptation of element shapes enables coordinated evolution between anatomical modules. Nat Ecol Evol 5, 1250–1258 (2021). https://doi.org/10.1038/s41559-021-01509-w

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