Low morphological disparity and decelerated rate of limb size evolution close to the origin of birds

Aug 30, 2023

Nature Ecology & Evolution (2023)Cite this article

Metrics details

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.

This is a preview of subscription content, access via your institution

Access Nature and 54 other Nature Portfolio journals

Get Nature+, our best-value online-access subscription

$29.99 / 30 days

cancel any time

Subscribe to this journal

Receive 12 digital issues and online access to articles

$119.00 per year

only $9.92 per issue

Rent or buy this article

Get just this article for as long as you need it

$39.95

Prices may be subject to local taxes which are calculated during checkout

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).

The R code used in the comparative analyses is archived and available on the OSF (https://osf.io/8n3wt/?view_only=753148d6a15f478e8fa027890b6b9bde).

Brusatte, S. L., O’Connor, J. K. & Jarvis, E. D. The origin and diversification of birds. Curr. Biol. 25, R888–R898 (2015).

Article CAS PubMed Google Scholar

Xu, X. et al. An integrative approach to understanding bird origins. Science 346, 1253293 (2014).

Article PubMed Google Scholar

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

Article Google Scholar

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

Article PubMed Google Scholar

Lee, M. S. Y., Cau, A., Naish, D. & Dyke, G. J. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345, 562–566 (2014).

Article CAS PubMed Google Scholar

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

Article PubMed Google Scholar

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

PubMed PubMed Central Google Scholar

Hedrick, B. P., Manning, P. L., Lynch, E. R., Cordero, S. A. & Dodson, P. The geometry of taking flight: limb morphometrics in Mesozoic theropods. J. Morphol. 276, 152–166 (2015).

Article PubMed Google Scholar

Benson, R. B. J. et al. Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage. PLoS Biol. 12, e1001853 (2014).

Article PubMed PubMed Central Google Scholar

Hone, D. W. E., Dyke, G. J., Haden, M. & Benton, M. J. Body size evolution in Mesozoic birds. J. Evol. Biol. 21, 618–624 (2008).

Article CAS PubMed Google Scholar

Butler, R. J. & Goswami, A. Body size evolution in Mesozoic birds: little evidence for Cope's rule. J. Evol. Biol. 21, 1673–1682 (2008).

Article CAS PubMed Google Scholar

Wang, M., O’Connor, J. K., Xu, X. & Zhou, Z. A new Jurassic scansoriopterygid and the loss of membranous wings in theropod dinosaurs. Nature 569, 256–259 (2019).

Article CAS PubMed Google Scholar

Xu, X. et al. Two Early Cretaceous fossils document transitional stages in alvarezsaurian dinosaur evolution. Curr. Biol. 28, 2853–2860 (2018).

Article CAS PubMed Google Scholar

Ruiz, J., Torices, A., Serrano, H. & López, V. The hand structure of Carnotaurus sastrei (Theropoda, Abelisauridae): implications for hand diversity and evolution in abelisaurids. Palaeontology 54, 1271–1277 (2011).

Article Google Scholar

Gatesy, S. M. Hind limb scaling in birds and other theropods: implications for terrestrial locomotion. J. Morphol. 209, 83–96 (1991).

Article PubMed Google Scholar

Allen, V. R., Kilbourne, B. M. & Hutchinson, J. R. The evolution of pelvic limb muscle moment arms in bird-line archosaurs. Sci. Adv. 7, eabe2778 (2021).

Article PubMed PubMed Central Google Scholar

Dececchi, T. A. & Larsson, H. C. E. Assessing arboreal adaptations of bird antecedents: testing the ecological setting of the origin of the avian flight stroke. PLoS ONE 6, e22292 (2011).

Article PubMed PubMed Central Google Scholar

Nudds, R. L., Dyke, G. J. & Rayner, J. M. V. Avian brachial index and wing kinematics: putting movement back into bones. J. Zool. 272, 218–226 (2007).

Article Google Scholar

Wang, X. & Clarke, J. A. Phylogeny and forelimb disparity in waterbirds. Evolution 68, 2847–2860 (2014).

Article PubMed Google Scholar

Pei, R. et al. Potential for powered flight neared by most close avialan relatives, but few crossed its thresholds. Curr. Biol. 30, 4033–4046 (2020).

Article CAS PubMed Google Scholar

Cooney, C. R. et al. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature 542, 344–347 (2017).

Article CAS PubMed PubMed Central Google Scholar

Erwin, D. H. Novelty and innovation in the history of life. Curr. Biol. 25, R930–R940 (2015).

Article CAS PubMed Google Scholar

Sullivan, C., Xu, X. & O’Connor, J. K. Complexities and novelties in the early evolution of avian flight, as seen in the Mesozoic Yanliao and Jehol Biotas of Northeast China. Palaeoworld 26, 212–229 (2017).

Article Google Scholar

Brusatte, S. L., Lloyd, G. T., Wang, S. C. & Norell, M. A. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur-bird transition. Curr. Biol. 24, 2386–2392 (2014).

Article CAS PubMed Google Scholar

Sullivan, C., Hone, D. W. E., Xu, X. & Zhang, F. The asymmetry of the carpal joint and the evolution of wing folding in maniraptoran theropod dinosaurs. Proc. Biol. Sci. 277, 2027–2033 (2010).

PubMed PubMed Central Google Scholar

Wang, M. & Zhou, Z. in The Biology of the Avian Respiratory System (ed. Maina N. J.) 1–26 (Springer International Publishing, 2017).

Chiappe, L. M. & Walker, C. A. in Mesozoic Birds: Above the Heads of Dinosaurs (eds Chiappe, L. M. & Witmer, L. M.) 240–267 (Univ. California Press, 2002).

Tobias, J. A. et al. AVONET: morphological, ecological and geographical data for all birds. Ecol. Lett. 25, 581–597 (2022).

Article PubMed Google Scholar

Dyke, G. J. & Nudds, R. L. The fossil record and limb disparity of enantiornithines, the dominant flying birds of the Cretaceous. Lethaia 42, 248–254 (2009).

Article Google Scholar

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

Wang, M. & Lloyd, G. T. Rates of morphological evolution are heterogeneous in Early Cretaceous birds. Proc. Biol. Sci. 283, 20160214 (2016).

PubMed PubMed Central Google Scholar

Zhang, C. & Wang, M. Bayesian tip dating reveals heterogeneous morphological clocks in Mesozoic birds. R. Soc. Open Sci. 6, 182062 (2019).

Article PubMed PubMed Central Google Scholar

Chiappe, L. M. The first 85 million years of avian evolution. Nature 378, 349–355 (1995).

Article CAS Google Scholar

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

Turner, A. H., Makovicky, P. J. & Norell, M. A. A review of dromaeosaurid systematics and paravian phylogeny. Bull. Am. Mus. Nat. Hist. 371, 1–206 (2012).

Article Google Scholar

Pol, D. & Goloboff, P. A. The impact of unstable taxa in coelurosaurian phylogeny and resampling support measures for parsimony analyses. Bull. Am. Mus. Nat. Hist. 440, 97–115 (2020).

Google Scholar

Wang, M., Lloyd, G. T., Zhang, C. & Zhou, Z. The patterns and modes of the evolution of disparity in Mesozoic birds. Proc. Biol. Sci. 288, 20203105 (2021).

PubMed PubMed Central Google Scholar

Lee, Y.-N. et al. Resolving the long-standing enigmas of a giant ornithomimosaur Deinocheirus mirificus. Nature 515, 257–260 (2014).

Article CAS PubMed Google Scholar

Rauhut, O. W. M. & Pol, D. Probable basal allosauroid from the early Middle Jurassic Cañadón Asfalto Formation of Argentina highlights phylogenetic uncertainty in tetanuran theropod dinosaurs. Sci. Rep. 9, 18826 (2019).

Article CAS PubMed PubMed Central Google Scholar

O’Connor, J. K. & Sullivan, C. Reinterpretation of the Early Cretaceous maniraptoran (Dinosauria: Theropoda) Zhongornis haoae as a scansoriopterygid-like non-avian, and morphological resemblances between scansoriopterygids and basal oviraptorosaurs. Vertebr. PalAsiat. 52, 3–30 (2014).

Google Scholar

Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

Article CAS PubMed Google Scholar

Bapst, D. W. paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3, 803–807 (2012).

Article Google Scholar

Stadler, T. Sampling-through-time in birth–death trees. J. Theor. Biol. 267, 396–404 (2010).

Article PubMed Google Scholar

Bapst, D. W. A stochastic rate-calibrated method for time-scaling phylogenies of fossil taxa. Methods Ecol. Evol. 4, 724–733 (2013).

Article Google Scholar

Ballell, A., Moon, B. C., Porro, L. B., Benton, M. J. & Rayfield, E. J. Convergence and functional evolution of longirostry in crocodylomorphs. Palaeontology 62, 867–887 (2019).

Article Google Scholar

Herrera-Flores, J. A., Stubbs, T. L. & Benton, M. J. Ecomorphological diversification of squamates in the Cretaceous. R. Soc. Open Sci. 8, 201961 (2021).

Article PubMed PubMed Central Google Scholar

Gavryushkina, A. & Zhang, C. in The Molecular Evolutionary Clock: Theory and Practice (ed. Ho, S. Y. W.) 175–193 (Springer, 2020).

Wright, A. M., Bapst, D. W., Barido-Sottani, J. & Warnock, R. C. M. Integrating fossil observations into phylogenetics using the fossilized birth–death model. Annu. Rev. Ecol. Evol. Syst. 53, 251–273 (2022).

Article Google Scholar

Benson, R. B. J., Godoy, P., Bronzati, M., Butler, R. J. & Gearty, W. Reconstructed evolutionary patterns for crocodile-line archosaurs demonstrate impact of failure to log-transform body size data. Commun. Biol. 5, 171 (2022).

Article PubMed PubMed Central Google Scholar

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

Article PubMed Google Scholar

Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

Article Google Scholar

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

Article CAS PubMed Google Scholar

Campione, N. E. & Evans, D. C. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biol. 10, 60 (2012).

Article PubMed PubMed Central Google Scholar

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

Article Google Scholar

Wills, M. A., Briggs, D. E. G. & Fortey, R. A. Disparity as an evolutionary index: a comparison of Cambrian and recent arthropods. Paleobiology 20, 93–130 (1994).

Article Google Scholar

Foote, M. Morphological and taxonomic diversity in a clade's history: the blastoid record and stochastic simulations. Contrib. Mus. Paleontol. Univ. Mich. 28, 101–140 (1991).

Google Scholar

Guillerme, T. dispRity: a modular R package for measuring disparity. Methods Ecol. Evol. 9, 1755–1763 (2018).

Article Google Scholar

Oksanen, J. et al. Package ‘vegan’. Community Ecology Package. R package version 2.6-2 https://cran.r-project.org/web/packages/vegan/vegan.pdf (2007).

Nudds, R. L., Dyke, G. J. & Rayner, J. M. V. Forelimb proportions and the evolutionary radiation of Neornithes. Proc. Biol. Sci. 271, S324–S327 (2004).

Article PubMed PubMed Central Google Scholar

Samuels, J. X. & Van Valkenburgh, B. Skeletal indicators of locomotor adaptations in living and extinct rodents. J. Morphol. 269, 1387–1411 (2008).

Article PubMed Google Scholar

Zeffer, A., Johansson, L. C. & Marmebro, Å. Functional correlation between habitat use and leg morphology in birds (Aves). Biol. J. Linn. Soc. Lond. 79, 461–484 (2003).

Article Google Scholar

Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R. News 6, 7–11 (2006).

Google Scholar

Felice, R. N. et al. Decelerated dinosaur skull evolution with the origin of birds. PLoS Biol. 18, e3000801 (2020).

Article CAS PubMed PubMed Central Google Scholar

Download references

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).

Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China

Min Wang & Zhonghe Zhou

You can also search for this author in PubMed Google Scholar

You can also search for this author in PubMed Google Scholar

M.W. conceived the project. M.W. and Z.Z. performed the analyses and wrote the manuscript.

Correspondence to Min Wang.

The authors declare no competing interests.

Nature Ecology & Evolution thanks Stephen Brusatte and Gregory Funston for their contribution to the peer review of this work.

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

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).

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.

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.

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.

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).

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).

Evolutionary changes of brachial index across time-calibrated Mesozoic theropod tree.

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.

Evolutionary changes of crural index across time-calibrated Mesozoic theropod tree.

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.

Supplementary Figs. 1–23 and Tables 1–11.

List of taxonomical sampling.

The R code, raw data and results derived from the phylogeny scaled using the ‘equal’ method, and different phylogenetic hypotheses.

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

Wang, M., Zhou, Z. Low morphological disparity and decelerated rate of limb size evolution close to the origin of birds. Nat Ecol Evol (2023). https://doi.org/10.1038/s41559-023-02091-z

Download citation

Received: 03 February 2023

Accepted: 09 May 2023

Published: 05 June 2023

DOI: https://doi.org/10.1038/s41559-023-02091-z

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative