Skip to main content

Thank you for visiting nature.com. 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.

  • Article
  • Published:

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

Nature Ecology & Evolution volume 7, pages 1257–1266 (2023)Cite this article

Subjects

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.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Fig. 1: Morphological disparity of appendicular elements of Mesozoic theropods.
Fig. 2: Patterns of morphological disparity in the forelimb and hindlimb among Mesozoic theropods.
Fig. 3: Evolutionary changes of two functional indices across the Mesozoic theropod phylogeny.
Fig. 4: Evolutionary rate and rate shift of appendicular elements in Mesozoic theropods.
Fig. 5: Evolutionary rate and rate shift of BI and CI across the Mesozoic theropod phylogeny.

Similar content being viewed by others

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).

References

  1. 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 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  5. 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 

  6. 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 

  7. 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 

  8. 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 

  9. 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 

  10. 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 

  11. 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 

  12. 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 

  13. 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 

  14. 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 

  15. 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 

  16. 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 

  17. 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 

  18. 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 

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

    Article  PubMed  Google Scholar 

  20. 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 

  21. 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 

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

    Article  CAS  PubMed  Google Scholar 

  23. 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 

  24. 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 

  25. 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 

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

  27. 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).

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

    Article  PubMed  Google Scholar 

  29. 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 

  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. 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 

  32. 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 

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

    Article  CAS  Google Scholar 

  34. 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 

  35. 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 

  36. 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 

  37. 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 

  38. 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 

  39. 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 

  40. 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 

  41. 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 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  44. 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 

  45. 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 

  46. 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 

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

  48. 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 

  49. 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 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  53. 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 

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

    Article  Google Scholar 

  55. 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 

  56. 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 

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

    Article  Google Scholar 

  58. 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).

  59. 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 

  60. 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 

  61. 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 

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

    Google Scholar 

  63. 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

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).

Author information

Authors and Affiliations

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

    Min Wang & Zhonghe Zhou

Authors
  1. Min Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhonghe Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

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

Corresponding author

Correspondence to Min Wang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

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

Additional information

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

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.

Supplementary information

Supplementary Information

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

Reporting Summary

Supplementary Table 1

List of taxonomical sampling.

Supplementary Code

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

Rights and permissions

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

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

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

Search

Advanced search

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