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Mega-evolutionary dynamics of the adaptive radiation of birds

A Corrigendum to this article was published on 29 November 2017

This article has been updated

Abstract

The origin and expansion of biological diversity is regulated by both developmental trajectories1,2 and limits on available ecological niches3,4,5,6,7. As lineages diversify, an early and often rapid phase of species and trait proliferation gives way to evolutionary slow-downs as new species pack into ever more densely occupied regions of ecological niche space6,8. Small clades such as Darwin’s finches demonstrate that natural selection is the driving force of adaptive radiations, but how microevolutionary processes scale up to shape the expansion of phenotypic diversity over much longer evolutionary timescales is unclear9. Here we address this problem on a global scale by analysing a crowdsourced dataset of three-dimensional scanned bill morphology from more than 2,000 species. We find that bill diversity expanded early in extant avian evolutionary history, before transitioning to a phase dominated by packing of morphological space. However, this early phenotypic diversification is decoupled from temporal variation in evolutionary rate: rates of bill evolution vary among lineages but are comparatively stable through time. We find that rare, but major, discontinuities in phenotype emerge from rapid increases in rate along single branches, sometimes leading to depauperate clades with unusual bill morphologies. Despite these jumps between groups, the major axes of within-group bill-shape evolution are remarkably consistent across birds. We reveal that macroevolutionary processes underlying global-scale adaptive radiations support Darwinian9 and Simpsonian4 ideas of microevolution within adaptive zones and accelerated evolution between distinct adaptive peaks.

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Figure 1: Bird bill morphospace density plots.
Figure 2: Morphospace filling through time.
Figure 3: Multivariate rates of bill-shape evolution.

Change history

  • 30 November 2017

    Please see accompanying Corrigendum (http://doi.org/10.1038/nature24665). Two missing Supplementary Information files (‘Prum_merge_taxonomy_CRC_v2.csv’ and ‘PrumTreeMerge_CRC_v1.csv’) have been added to this Letter.

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Acknowledgements

We thank M. Adams, H. van Grouw and R. Prys-Jones from the Bird Group at the NHM, Tring and H. McGhie at the Manchester Museum for providing access to and expertise in the collections; S. Meiri of Tel Aviv University for providing a sample of study skins; S. Stone of MechInovation Ltd for providing training and advice on 3D scanning; M. Groves, J. McLaughlin and M. Pidd of HRI Digital for the construction of http://www.markmybird.org; A. Beckerman for advice on analysing P matrices; E. Rayfield, A. Pigot, A. Mooers and A. White for providing valuable comments on pre-submission drafts of the manuscript. Finally, we are indebted to the volunteer citizen scientists at http://www.markmybird.org for helping to build the database of bird bill shape and contribute to our understanding of avian evolution. This work was funded by the European Research Council (grant number 615709 Project ‘ToLERates’) and by a Royal Society University Research Fellowship to G.H.T. (UF120016).

Author information

Authors and Affiliations

Authors

Contributions

C.R.C., J.A.B. and G.H.T. conceived the study, designed analytical protocols, analysed the data and wrote the manuscript. All authors collected and processed data and provided input to the manuscript.

Corresponding author

Correspondence to Gavin H. Thomas.

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Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks D. Rabosky and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Figure 1 Positions of landmarks and semi-landmarks.

The image shows a 3D scan of a shoebill (Balaeniceps rex) bill marked up with four fixed landmarks (numbered red points) and three semi-landmark curves along the dorsal profile (from points 1 to 2) and tomial edges (left from point 1 to 3 and right from point 1 to 4). Each curve consists of 25 semi-landmarks (black points).

Extended Data Figure 2 Morphospace density through time.

ah, Plots show the filling of avian bill morphospace through time (n = 2,028 species) for PCs 1 (a), 2 (b), 3 (c), 4 (d), 5 (e), 6 (f), 7 (g) and 8 (h). Densities were calculated in 1-million-year time slices on the basis of univariate rate heterogeneous models of trait evolution using a stage 2 Hackett MCC tree from http://www.birdtree.org. The scale runs from low density (blue) to high density (red), indicating the extent of niche packing through time in different regions of bill morphospace. For each axis, the frequency distribution of PC scores among species is also shown (grey bars).

Extended Data Figure 3 Comparison of multivariate rates of bill-shape evolution and disparity through time for alternative datasets.

The plot shows estimates of the mean relative multivariate rate of bill-shape evolution for four alternative versions of the avian phylogeny and also when using phylogenetic principal components (pPCs) (see Methods). Shown below are plots comparing estimates of disparity and rates through time derived from each dataset. For stage 2 trees n = 2,028 species and for stage 1 trees n = 1,627 species.

Extended Data Figure 4 Multivariate rates of bill-shape evolution for a composite tree based on the Prum et al. backbone.

a, The avian phylogeny coloured according to estimates of the mean relative multivariate rate of bill-shape evolution. Grey triangles show the stem branch of clades with support for whole clade shifts in evolutionary rate. Coloured circles show rate shifts on individual internal branches (colour indicates the rate estimate). The relative size of triangles and circles indicates the posterior probability (PP) of a rate shift. Filled and open triangles distinguish between shifts on the focal node (filled) and shifts that occur either at the focal node or on one of the two immediate daughter nodes (open). b, Accumulation of multivariate disparity through time in 1 million year time slices (thick black line: observed data; thin black line: after LOESS smoothing; blue lines: constant rate null model; red lines: variable rate null model). c, Comparison of slopes (estimated in 5 million year windows) of the LOESS-smoothed observed data and null models. Differences in slope above and below zero indicate dominance of morphospace expansion versus morphospace packing, respectively. Shading indicates 95% confidence intervals. d, Mean relative rates of evolution with 95% confidence intervals (grey) through time.

Extended Data Figure 5 Phylogenetic mapping of univariate rates of bill-shape evolution.

The plots shows the avian phylogeny of all taxa included in the study (n = 2,028 species) with branches coloured on a common scale across panels according to estimates of the univariate rate of bill-shape evolution. ah, PC1 (a), PC2 (b), PC3 (c), PC4 (d), PC5 (e), PC6 (f), PC7 (g) and PC8 (h).

Extended Data Figure 6 Morphospaces of avian higher taxa.

Pairwise scatter plots of PCs 1 and 2, 3 and 4, 5 and 6, and 7 and 8 showing focal higher taxa (non-passerines, purple; passerines, green) against total avian morphospace (grey). Values in parentheses show the number of species sampled.

Extended Data Figure 7 Morphological subspaces of the P of avian higher taxa.

The figure shows representations of P for avian higher taxa with ≥ 20 species sampled. First column: distribution of species values on each of the first eight raw PCs showing variation in morphospace centroid for each higher taxon. Second column: two-dimensional subspace for each taxon with non-passerine (purple) and passerine (green) subspaces. The x and y axes follow the global leading (Pmax) and secondary eigenvectors. Third column: percentage of total variance explained and individual PC loadings onto each taxon specific Pmax. Inset: 3D subspace for all non-passerines (purple) and passerines (green). Values in parentheses show the number of species sampled.

Extended Data Table 1 Variance, repeatability and phylogenetic signal of PC axes
Extended Data Table 2 Summary of major single-lineage bill evolutionary rate shifts
Extended Data Table 3 Comparison of trait models

Related audio

Supplementary information

Supplementary Data

This file details the mapping of Jetz et al. clades to the Prum et al. backbone phylogeny. The table shows the nodes used to attach patch clades from the Jetz et al. stage 2 Hackett tree to the Prum et al. backbone phylogeny. (XLSX 42 kb)

Supplementary Data

This archive contains data files and an R script to combine the backbone (approximately family level) phylogeny of Prum et al. with the species level resolution of the Jetz et al. avian phylogeny. (ZIP 794 kb)

Supplementary Data

This archive contains all alternative genus level phylogenies used in the analyses. (ZIP 253 kb)

Supplementary Data

This file contains the source data for Extended Data Table 1. (CSV 334 kb)

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Cooney, C., Bright, J., Capp, E. et al. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature 542, 344–347 (2017). https://doi.org/10.1038/nature21074

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