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Environmental signal in the evolutionary diversification of bird skeletons

Nature volume 611, pages 306–311 (2022)Cite this article

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Abstract

Characterizing how variation in the tempo and mode of evolution has structured the phenotypic diversity of extant species is a central goal of macroevolution1,2,3. However, studies are typically limited to a handful of traits4,5,6, providing incomplete information. We analyse morphological diversification in living birds, an ecologically diverse group7, documenting structural scales from ‘pan-skeletal’ proportions down to the localized three-dimensional shape changes of individual bones. We find substantial variation in evolutionary modes among avian subgroups and among skeletal parts, indicating widespread mosaicism and possible differences in the structure of the macroevolutionary landscape across Earth’s main environments. Water-linked groups, especially Aequorlitornithes (waterbirds), have repeatedly explored a large portion of their total morphospace, emphasizing variation in body proportions and in the shape of bones close to the body core, which are functionally related to the mechanics of locomotion8. By contrast, landbirds (Inopinaves) evolved distinct, group-specific body forms early in the aftermath of the K-Pg and subsequently emphasized local shape variation, especially in the head and distal limb bones, which interact more directly with the environment. Passerines, which comprise more than half of all bird species, show a conservative evolutionary dynamic that resulted in low disparity across all skeletal parts. Evidence for early establishment of the morphospace of living birds is clear for some skeletal parts, including beaks and the combined skeletal morphology. However, we find little evidence for early partitioning of that morphospace, contrary to more specific predictions of ‘niche-filling’ models1,9. Nevertheless, early divergence among broad environmental types may have caused an early divergence of evolutionary modes, suggesting an important role for environmental divergence in structuring the radiation of crown-group birds.

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Fig. 1: Early establishment of the morphospace for skeletal form and beak shape during the diversification of Neornithes.
Fig. 2: Whole skeletal subclade disparity–age plotted across avian phylogeny and through time.
Fig. 3: Tests of early partitioning of avian skeletal space using the MDI.
Fig. 4: Deviations of group-specific disparities from the disparity expected if all birds were evolving under a uniform Brownian motion model of evolution.

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Data availability

Raw landmark coordinates can be accessed as Supplementary Files linked to this article and accessing our project in OSF Public Repository following this link: https://osf.io/wjk3m/. All three-dimensional meshes can be freely downloaded following the links to Morphosource in Supplementary Materials Table 1.

Code availability

Custom code can be accessed in our project in OSF Public Repository following this link: https://osf.io/wjk3m/.

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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 are grateful to A. Martin-Serra, J. L. Cantalapiedra, F. Blanco, M. Fabbri, I. Menéndez, S.M. Nebreda, J. Clavel, E.M. Steell, J. Marugán-Lobón and C. Navalón for enlightening discussion on contents, narrative and analytical approaches. We thank L. Balsa Pascual and Ó. Sanisidro for discussion on design choices. This work was supported by the European Union’s Horizon 2020 research and innovation programme 2014–2018 under grant agreement no. 677774 (European Research Council Starting grant no. TEMPO). Grant no. 677774 applies to the work of G.N., A.B. and R.B.J.B. G.N. acknowledges support from UKRI Future Leaders Fellowship no. MR/S032177/1.

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Authors and Affiliations

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

    Guillermo Navalón

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

    Guillermo Navalón, Alexander Bjarnason, Elizabeth Griffiths & Roger B. J. Benson

  3. Unidad de Paleontología, Departamento de Biología, Universidad Autónoma de Madrid, Madrid, Spain

    Guillermo Navalón

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Contributions

G.N. and R.B.J.B. conceptualized the study and designed the analytical approach. G.N., A.B., E.G. and R.B.J.B. collected and curated the data. G.N. and R.B.J.B. undertook the formal analyses. G.N. and R.B.J.B. wrote the manuscript. G.N. made the figures. G.N., A.B., E.G. and R.B.J.B. edited the text. R.B.J.B. acquired the funding used for this research.

Corresponding authors

Correspondence to Guillermo Navalón or Roger B. J. Benson.

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Nature thanks Gavin Thomas 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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Extended data figures and tables

Extended Data Fig. 1 Infographic displaying the data and the methods’ pipeline used in this study.

A detailed account of the Material and Methods used in our study can be found in the main text.

Extended Data Fig. 2 Diagram showing how subclade disparity through time is calculated as test of early partitioning of morphospace, showing idealized contrasting patterns of morphological evolution.

a) Example time-calibrated phylogeny and points in time (cladogenesis events) for which b) subclade disparities values are calculated for a Brownian model of diffusive evolution and two alternative modes of morphological evolution. c) Corresponding patterns in morphospace exploration over time for two idealised patterns of morphological evolution: early partitioning of trait space (morphospace) in which morphological evolution is constrained at the level of subclades, and a non-partitioned pattern in which constraints are similar in the total group and within subclades.

Extended Data Fig. 3 Tests of early-partitioning of avian allometry-free shape and local shape variation of the individual elements in Aequorlithornithes, Inopinaves and Passeriformes.

See Extended Data Fig. 2 for a detailed account of the idealised patterns associated with each mode of evolution of disparity through time.

Extended Data Fig. 4 Deviations of group-specific disparities from the disparity expected if all birds were evolving under a uniform Brownian motion model of evolution for additional groups of water-based (Gruiformes, Anseriformes) and land-based (non-landbird terrestrial Neoaves, Galliformes) birds.

Boxplots summarize the distribution of delta disparities, calculated as empirical disparities minus disparities for the 200 simulated values for each of the three target clades. All partitions and data types are displayed, namely, the whole skeleton, three main skeletal regions and individual bones and the four different aspects of morphological variation in the three target lineages of birds. Arrows highlight the lineage/partition/data type which shows particularly high (up pointing arrows) or low (down pointing arrows) values. Values are normalised by interquartile range.

Extended Data Fig. 5 Subclade disparity–age plots for the whole skeleton and body regions for Aequorlitornithes (waterbirds).

X axes represent subclade disparities while y axes represent time in millions of years from the present time. Solid coloured lines represent mean empirical disparities through time, dashed lines represent mean BM-simulated disparities through time, shaded polygons display the space between 95% percentile and 5% percentiles of disparities through time for BM-simulated data. Colour code of individual subclade disparities (dots) as in Fig. 2.

Extended Data Fig. 6 Subclade disparity–age plots for the whole skeleton and body regions for Inopinaves (landbirds).

X axes represent subclade disparities while y axes represent time in millions of years from the present time. Solid coloured lines represent mean empirical disparities through time, dashed lines represent mean BM-simulated disparities through time, shaded polygons display the space between 95% percentile and 5% percentiles of disparities through time for BM-simulated data. Colour code of individual subclade disparities (dots) as in Fig. 2.

Extended Data Fig. 7 Subclade disparity–age plots for the whole skeleton and body regions for Passeriformes (passerines).

X axes represent subclade disparities while y axes represent time in millions of years from the present time. Solid coloured lines represent mean empirical disparities through time, dashed lines represent mean BM-simulated disparities through time, shaded polygons display the space between 95% percentile and 5% percentiles of disparities through time for BM-simulated data. Colour code of individual subclade disparities (dots) as in Fig. 2.

Extended Data Fig. 8 Subclade disparity–age plots for the individual elements for Aequorlitornithes (waterbirds).

X axes represent subclade disparities while y axes represent time in millions of years from the present time. Solid coloured lines represent mean empirical disparities through time, dashed lines represent mean BM-simulated disparities through time, shaded polygons display the space between 95% percentile and 5% percentiles of disparities through time for BM-simulated data. Colour code of individual subclade disparities (dots) as in Fig. 2.

Extended Data Fig. 9 Subclade disparity–age plots for the individual elements for Inopinaves (landbirds).

X axes represent subclade disparities while y axes represent time in millions of years from the present time. Solid coloured lines represent mean empirical disparities through time, dashed lines represent mean BM-simulated disparities through time, shaded polygons display the space between 95% percentile and 5% percentiles of disparities through time for BM-simulated data. Colour code of individual subclade disparities (dots) as in Fig. 2.

Extended Data Fig. 10 Subclade disparity–age plots for the individual elements for Passeriformes (passerines).

X axes represent subclade disparities while y axes represent time in millions of years from the present time. Solid coloured lines represent mean empirical disparities through time, dashed lines represent mean BM-simulated disparities through time, shaded polygons display the space between 95% percentile and 5% percentiles of disparities through time for BM-simulated data. Colour code of individual subclade disparities (dots) as in Fig. 2.

Supplementary information

Supplementary Information

This file contains Supplementary Figs. 1–37 and References.

Reporting Summary

Peer Review File

Supplementary Table 1

List of specimens used in this study.

Supplementary Table 2

ANOVA tables used for proportions-normalizing individual elements.

Supplementary Table 3

Pairs of landmarks used to calculate maximum distances in each of the spatial axes.

Supplementary File 1

Bird_landmarks_Navalon_2022. Raw landmark coordinates for all specimens used in this study.

Supplementary File 2

Read_bird_landmarks_Navalon_2022. R code to read the raw landmarks coordinates in Supplementary File 1.

Supplementary File 3

Bird_processed_landmarks_Navalon_2022. Allometry-free and proportions free landmark coordinates for all specimens used in this study.

Supplementary File 4

Read_bird_processed_landmarks_Navalon_2022. R code to read the raw landmarks coordinates in Supplementary File 3.

Supplementary File 5

Combined phylogeny used in this study.

Supplementary File 6

Custom R functions used in this study.

Supplementary File 7

Custom R code used in this study.

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Navalón, G., Bjarnason, A., Griffiths, E. et al. Environmental signal in the evolutionary diversification of bird skeletons. Nature 611, 306–311 (2022). https://doi.org/10.1038/s41586-022-05372-y

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