Abstract
The origin of birds from theropod dinosaurs involves many changes in musculoskeletal anatomy and epidermal structures, including multiple instances of convergence and homology-related traits that contribute to the refinement of flight capability. Changes in limb sizes and proportions are important for locomotion (for example, the forelimb for bird flight); thus, understanding these patterns is central to investigating the transition from terrestrial to volant theropods. Here we analyse the patterns of morphological disparity and the evolutionary rate of appendicular limbs along avialan stem lineages using phylogenetic comparative approaches. Contrary to the traditional wisdom that an evolutionary innovation like flight would promote and accelerate evolvability, our results show a shift to low disparity and decelerated rate near the origin of avialans that is largely ascribed to the evolutionarily constrained forelimb. These results suggest that natural selection shaped patterns of limb evolution close to the origin of avialans in a way that may reflect the winged forelimb ‘blueprint’ associated with powered flight.
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Data availability
Supplementary material is available online. The R code, raw data and results derived from the phylogeny scaled using the ‘equal’ method, and the different phylogenetic hypotheses are available on the OSF (https://osf.io/8n3wt/?view_only=753148d6a15f478e8fa027890b6b9bde).
Code availability
The R code used in the comparative analyses is archived and available on the OSF (https://osf.io/8n3wt/?view_only=753148d6a15f478e8fa027890b6b9bde).
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Acknowledgements
We thank R. N. Felice for help in calculating the evolutionary rates in R. This research is supported by the National Natural Science Foundation of China (nos. 42225201 and 42288201), the Key Research Program of Frontier Sciences, the Chinese Academy of Sciences (no. ZDBS-LY-DQC002) and the Tencent Foundation (through the XPLORER PRIZE).
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M.W. conceived the project. M.W. and Z.Z. performed the analyses and wrote the manuscript.
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Extended data
Extended Data Fig. 1 Evolutionary changes of all appendicular elements across Mesozoic theropod phylogeny.
The first and third principal components (PCs) derived from pPCA of all limbs are mapped on the time-calibrated tree. a, PC1 (=70.03% variances). b, PC3 (=6.7% variances).
Extended Data Fig. 2 Phylomorphospace of forelimb morphological disparity of Mesozoic theropods.
The first three principal components (PCs) derived from pPCA of forelimb are used. a, Binary plot of PCs 1 and 2. b, Binary plot of PCs 1 and 3.
Extended Data Fig. 3 Phylomorphospace of hindlimb morphological disparity of Mesozoic theropods.
The first three principal components (PCs) derived from pPCA of hindlimb are used. a, Binary plot of PCs 1 and 2. b, Binary plot of PCs 1 and 3.
Extended Data Fig. 4 Rarefaction of disparity curves of Mesozoic theropods showing that the results are not strongly affected by sampling bias.
Morphological disparity is quantified using three metrices: a, sum of variances; b, median distance from centroid; c, and sum of ranges. The dark and light surfaces indicate the 50% and 95% confidence intervals, respectively.
Extended Data Fig. 5 Evolutionary changes of brachial (BI) and crural (CI) indices across Mesozoic theropod phylogeny.
a, Phylomorphospace of BI and crural CI indices with phylogeny accounted. b, c, Comparison of disparity among three subgroups using standard deviations of BI (b) and CI (c), respectively (The boxes represent the median, the first and the third quartile of the morphological disparity; n = 109 species). Morphological disparity was compared using Welch’s t-test for statistical significance (****two-sided p-value threshold <0.05).
Extended Data Fig. 6 Comparison of evolutionary rate of subgroups of Mesozoic theropods.
Evolutionary rates are significantly different in all pairwise comparisons. The mean rate scalar is the mean of the rate scalars calculated in the post-burn-in posterior distribution under the variable rate evolutionary model (The boxes represent the median, the first and the third quartile of the mean rate scalar; n = 109 species). a, All appendicular elements. b, Forelimb. c, Hindlimb. Evolutionary rate among subgroups were compared using a nonparametric t-test for statistical significance (****: p < 0.00005).
Extended Data Fig. 7
Evolutionary changes of brachial index across time-calibrated Mesozoic theropod tree.
Extended Data Fig. 8 Evolutionary changes of brachial index across Mesozoic theropod phylogeny.
a, Branch specific evolutionary rates and rate shifts (Branch specific evolutionary rates are denoted by the color gradients. Posterior probabilities of rate shifts are indicated by the relative size of the grey triangles). b, Comparison of evolutionary rate of brachial index among subgroups (The boxes represent the median, the first and the third quartile of the mean rate scalar; n = 109 species). Evolutionary rates are significantly different in all pairwise comparisons except between Avialae and non-paravian theropods.
Extended Data Fig. 9
Evolutionary changes of crural index across time-calibrated Mesozoic theropod tree.
Extended Data Fig. 10 Evolutionary changes of crural index across Mesozoic theropod phylogeny.
a, Branch specific evolutionary rates and rate shifts (Branch specific evolutionary rates are denoted by the color gradients. Posterior probabilities of rate shifts are indicated by the relative size of the grey triangles). b, Comparison of evolutionary rate of brachial index among subgroups (The boxes represent the median, the first and the third quartile of the mean rate scalar; n = 109 species). Evolutionary rates are significantly different in all pairwise comparisons.
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Supplementary Figs. 1–23 and Tables 1–11.
Supplementary Table 1
List of taxonomical sampling.
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The R code, raw data and results derived from the phylogeny scaled using the ‘equal’ method, and different phylogenetic hypotheses.
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Wang, M., Zhou, Z. Low morphological disparity and decelerated rate of limb size evolution close to the origin of birds. Nat Ecol Evol 7, 1257–1266 (2023). https://doi.org/10.1038/s41559-023-02091-z
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DOI: https://doi.org/10.1038/s41559-023-02091-z
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