Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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


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.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.

Data availability

The specimen sources, scan parameters and metadata are reported in the Supplementary Information. All scans and 3D objects are available at, 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.


  1. 1.

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

    Article  Google Scholar 

  2. 2.

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

    Article  PubMed  Google Scholar 

  3. 3.

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

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Klingenberg, C. P. Morphological integration and developmental modularity. Annu. Rev. Ecol. Evol. Syst. 39, 115–132 (2008).

    Article  Google Scholar 

  5. 5.

    Klingenberg, C. P. Studying morphological integration and modularity at multiple levels: concepts and analysis. Phil. Trans. R. Soc. B 369, 20130249 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    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 

  7. 7.

    Olson, E. & Miller, R. Morphological Integration (Univ. of Chicago Press, 1958).

  8. 8.

    Pigliucci, M. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecol. Lett. 6, 265–272 (2003).

    Article  Google Scholar 

  9. 9.

    Eble, G. J. in Phenotypic Integration: Studying the Ecology and Evolution of Complex Phenotypes (eds Pigliucci, M. & Preston, K.) 253–273 (Oxford Univ. Press, 2004).

  10. 10.

    Goswami, A., Smaers, J. B., Soligo, C. & Polly, P. D. The macroevolutionary consequences of phenotypic integration: from development to deep time. Phil. Trans. R. Soc. B 369, 20130254 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Goswami, A., Binder, W. J., Meachen, J. & O’Keefe, F. R. The fossil record of phenotypic integration and modularity: a deep-time perspective on developmental and evolutionary dynamics. Proc. Natl Acad. Sci. USA 112, 4891–4896 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Wagner, G. P. & Schwenk, K. Evolutionarily stable configurations: functional integration and the evolution of phenotypic stability. Evol. Biol. 31, 155–217 (2000).

    Google Scholar 

  13. 13.

    Hallgrímsson, B., Willmore, K. & Hall, B. K. Canalization, developmental stability, and morphological integration in primate limbs. Am. J. Phys. Anthropol. 119, 131–158 (2002).

    Article  Google Scholar 

  14. 14.

    Gould, S. J. A developmental constraint in cerion, with comments on the definition and interpretation of constraint in evolution. Evolution 43, 516–539 (1989).

    PubMed  Google Scholar 

  15. 15.

    Arthur, W. Developmental drive: an important determinant of the direction of phenotypic evolution. Evol. Dev. 3, 271–278 (2001).

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Klingenberg, C. P. in Variation: A Central Concept in Biology (eds Hallgrímsson, B. & Hall, B.) 219–247 (Elsevier, 2005).

  17. 17.

    Felice, R. N. & Goswami, A. Developmental origins of mosaic evolution in the avian cranium. Proc. Natl Acad. Sci. USA 115, 555–560 (2018).

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Bell, E., Andres, B. & Goswami, A. Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats. J. Evol. Biol. 24, 2586–2599 (2011).

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Gatesy, S. M. & Dial, K. P. Locomotor modules and the evolution of avian flight. Evolution 50, 331–340 (1996).

    Article  PubMed  Google Scholar 

  20. 20.

    Gatesy, S. M. & Middleton, K. M. Bipedalism, flight, and the evolution of theropod locomotor diversity. J. Vertebr. Paleontol. 17, 308–329 (1997).

    Article  Google Scholar 

  21. 21.

    Kulemeyer, C., Asbahr, K., Gunz, P., Frahnert, S. & Bairlein, F. Functional morphology and integration of corvid skulls—a 3D geometric morphometric approach. Front. Zool. 6, 2 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Bright, J. A., Marugán-Lobón, J., Rayfield, E. J. & Cobb, S. N. The multifactorial nature of beak and skull shape evolution in parrots and cockatoos (Psittaciformes). BMC Evol. Biol. 19, 104 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Bright, J. A., Marugán-Lobón, J., Cobb, S. N. & Rayfield, E. J. The shapes of bird beaks are highly controlled by nondietary factors. Proc. Natl Acad. Sci. USA 113, 5352–5357 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Navalón, G., Marugán-Lobón, J., Bright, J. A., Cooney, C. R. & Rayfield, E. J. The consequences of craniofacial integration for the adaptive radiations of Darwin’s finches and Hawaiian honeycreepers. Nat. Ecol. Evol. 4, 270–278 (2020).

    Article  PubMed  Google Scholar 

  25. 25.

    Felice, R. N., Randau, M. & Goswami, A. A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution 72, 2580–2594 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Shatkovska, O. V. & Ghazali, M. Integration of skeletal traits in some passerines: impact (or the lack thereof) of body mass, phylogeny, diet and habitat. J. Anat. 236, 274–287 (2020).

    Article  PubMed  Google Scholar 

  27. 27.

    Hieronymus, T. L. Qualitative skeletal correlates of wing shape in extant birds (Aves: Neoaves). BMC Evol. Biol. 15, 30 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Felice, R. N., Tobias, J. A., Pigot, A. L. & Goswami, A. Dietary niche and the evolution of cranial morphology in birds. Proc. R. Soc. B 286, 20182677 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Navalón, G., Bright, J. A., Marugán-Lobón, J. & Rayfield, E. J. The evolutionary relationship among beak shape, mechanical advantage, and feeding ecology in modern birds. Evolution 73, 422–435 (2019).

    Article  PubMed  Google Scholar 

  30. 30.

    Pigot, A. L. et al. Macroevolutionary convergence connects morphological form to ecological function in birds. Nat. Ecol. Evol. 4, 230–239 (2020).

    Article  PubMed  Google Scholar 

  31. 31.

    Grant, R. B. & Grant, P. R. What Darwin’s finches can teach us about the evolutionary origin and regulation of biodiversity. BioScience 53, 965–975 (2003).

    Article  Google Scholar 

  32. 32.

    Van de Ven, T., Martin, R., Vink, T., McKechnie, E. & Cunningham, S. Regulation of heat exchange across the hornbill beak: functional similarities with toucans? PLoS ONE 11, e0154768 (2016).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Lamichhaney, S. et al. Rapid hybrid speciation in Darwin’s finches. Science 359, 224–228 (2018).

    CAS  Article  Google Scholar 

  34. 34.

    Klingenberg, C. P. & Marugán-Lobón, J. Evolutionary covariation in geometric morphometric data: analyzing integration, modularity, and allometry in a phylogenetic context. Syst. Biol. 62, 591–610 (2013).

    Article  Google Scholar 

  35. 35.

    Dececchi, T. A. & Larsson, H. C. Body and limb size dissociation at the origin of birds: uncoupling allometric constraints across a macroevolutionary transition. Evolution 67, 2741–2752 (2013).

    Article  Google Scholar 

  36. 36.

    Nudds, R., Dyke, G. & Rayner, J. Forelimb proportions and the evolutionary radiation of Neornithes. Proc. R. Soc. Lond. B 271, S324–S327 (2004).

    Google Scholar 

  37. 37.

    Benson, R. B. & Choiniere, J. N. Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds. Proc. R. Soc. B 280, 20131780 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Videler, J. J. Avian Flight (Oxford Univ. Press, 2006).

  39. 39.

    Carrano, M. T. & Sidor, C. A. Theropod hind limb disparity revisited: comments on Gatesy and Middleton (1997). J. Vertebr. Paleontol. 19, 602–605 (1999).

    Article  Google Scholar 

  40. 40.

    Middleton, K. M. & Gatesy, S. M. Theropod forelimb design and evolution. Zool. J. Linn. Soc. 128, 149–187 (2000).

    Article  Google Scholar 

  41. 41.

    Young, N. M., Linde-Medina, M., Fondon, J. W., Hallgrímsson, B. & Marcucio, R. S. Craniofacial diversification in the domestic pigeon and the evolution of the avian skull. Nat. Ecol. Evol. 1, 0095 (2017).

    Article  Google Scholar 

  42. 42.

    Martín-Serra, A. & Benson, R. B. Developmental constraints do not influence long-term phenotypic evolution of marsupial forelimbs as revealed by interspecific disparity and integration patterns. Am. Nat. 195, 547–560 (2020).

    Article  PubMed  Google Scholar 

  43. 43.

    Dumont, E. R. et al. Selection for mechanical advantage underlies multiple cranial optima in New World leaf-nosed bats. Evolution 68, 1436–1449 (2014).

    Article  PubMed  Google Scholar 

  44. 44.

    Hedrick, B. P. et al. Morphological diversification under high integration in a hyper diverse mammal clade. J. Mamm. Evol. 27, 563–575 (2020).

    Article  Google Scholar 

  45. 45.

    Rossoni, D. M., Costa, B. M., Giannini, N. P. & Marroig, G. A multiple peak adaptive landscape based on feeding strategies and roosting ecology shaped the evolution of cranial covariance structure and morphological differentiation in phyllostomid bats. Evolution 73, 961–981 (2019).

    Article  PubMed  Google Scholar 

  46. 46.

    Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Bjarnason, A. & Benson, R. A 3D geometric morphometric dataset quantifying skeletal variation in birds. MorphoMuseuM 7, e125 (2021).

    Article  Google Scholar 

  48. 48.

    Adams, D. C., Rohlf, F. J. & Slice, D. E. Geometric morphometrics: ten years of progress following the ‘revolution’. Ital. J. Zool. 71, 5–16 (2004).

    Article  Google Scholar 

  49. 49.

    R Core Team R: A Language and Environment for Statistical Computing v.3.6.3 (R Foundation for Statistical Computing, 2020).

  50. 50.

    Birds of the World (The Cornell Lab of Ornithology, 2021);

  51. 51.

    Dunning, J. B. Jr CRC Handbook of Avian Body Masses (CRC, 1992).

  52. 52.

    The IUCN Red List of Threatened Species (IUCN, 2019);

  53. 53.

    Wilman, H. et al. EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95, 2027 (2014).

    Article  Google Scholar 

  54. 54.

    Taylor, G. & Thomas, A. Evolutionary Biomechanics (Oxford Univ. Press, 2014).

  55. 55.

    Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M. & Hornik, K. cluster: Cluster analysis basics and extensions. R package version 2.1.0 (2019).

  56. 56.

    Grafen, A. The phylogenetic regression. Phil. Trans. R. Soc. Lond. B 326, 119–157 (1989).

    CAS  Article  Google Scholar 

  57. 57.

    Revell, L. J. Size-correction and principal components for interspecific comparative studies. Evolution 63, 3258–3268 (2009).

    Article  PubMed  Google Scholar 

  58. 58.

    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team nlme: Linear and nonlinear mixed effects models. R package version 3.1-145 (2020).

  59. 59.

    Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2018).

    Article  CAS  Google Scholar 

  60. 60.

    Goodall, C. Procrustes methods in the statistical analysis of shape. J. R. Stat. Soc. B 53, 285–321 (1991).

    Google Scholar 

  61. 61.

    Adams, D., Collyer, M. & Kaliontzopoulou, A. Geomorph: Software for geometric morphometric analyses. R package version 3.2.1 (2020).

  62. 62.

    Felsenstein, J. Phylogenies and the comparative method. Am. Nat. 125, 1–15 (1985).

    Article  Google Scholar 

  63. 63.

    Adams, D. C. & Felice, R. N. Assessing trait covariation and morphological integration on phylogenies using evolutionary covariance matrices. PLoS ONE 9, e94335 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    Rohlf, F. J. & Corti, M. Use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49, 740–753 (2000).

    CAS  Article  PubMed  Google Scholar 

  65. 65.

    Adams, D. C. & Collyer, M. L. On the comparison of the strength of morphological integration across morphometric datasets. Evolution 70, 2623–2631 (2016).

    Article  PubMed  Google Scholar 

  66. 66.

    Melo, D., Garcia, G., Hubbe, A., Assis, A. P. & Marroig, G. Evolqg—an R package for evolutionary quantitative genetics [version 3; referees: 2 approved, 1 approved with reservations]. F1000Research 4, 925 (2015).

    Article  PubMed  Google Scholar 

  67. 67.

    Goswami, A. & Polly, P. D. Methods for studying morphological integration and modularity. Paleontol. Soc. Pap. 16, 213–243 (2010).

    Article  Google Scholar 

  68. 68.

    Oksanen, J. et al. vegan: Community ecology package. R package version 2.5-6 (2019).

Download references


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.

Author information




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.

Corresponding author

Correspondence to Andrew Orkney.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review informationNature 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.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

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

Reporting Summary

Peer Review Information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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).

Download citation


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing