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Linking the evolution of body shape and locomotor biomechanics in bird-line archosaurs

Nature volume 497, pages 104–107 (2013)Cite this article

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Abstract

Locomotion in living birds (Neornithes) has two remarkable features: feather-assisted flight, and the use of unusually crouched hindlimbs for bipedal support and movement. When and how these defining functional traits evolved remains controversial1,2,3,4,5,6,7,8. However, the advent of computer modelling approaches and the discoveries of exceptionally preserved key specimens now make it possible to use quantitative data on whole-body morphology to address the biomechanics underlying this issue. Here we use digital body reconstructions to quantify evolutionary trends in locomotor biomechanics (whole-body proportions and centre-of-mass position) across the clade Archosauria. We use three-dimensional digital reconstruction to estimate body shape from skeletal dimensions for 17 archosaurs along the ancestral bird line, including the exceptionally preserved, feathered taxa Microraptor, Archaeopteryx, Pengornis and Yixianornis, which represent key stages in the evolution of the avian body plan. Rather than a discrete transition from more-upright postures in the basal-most birds (Avialae) and their immediate outgroup deinonychosauria5,6, our results support hypotheses of a gradual, stepwise acquisition of more-crouched limb postures across much of theropod evolution1,2,3,4, although we find evidence of an accelerated change within the clade Maniraptora (birds and their closest relatives, such as deinonychosaurs). In addition, whereas reduction of the tail is widely accepted to be the primary morphological factor correlated with centre-of-mass position and, hence, evolution of hindlimb posture1,2,3,4,5,6,7,8, we instead find that enlargement of the pectoral limb and several associated trends have a much stronger influence. Intriguingly, our support for the onset of accelerated morpho-functional trends within Maniraptora is closely correlated with the evolution of flight. Because we find that the evolution of enlarged forelimbs is strongly linked, via whole-body centre of mass, to hindlimb function during terrestrial locomotion, we suggest that the evolution of avian flight is linked to anatomical novelties in the pelvic limb as well as the pectoral.

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Figure 1: Dorsal views of models of study taxa, arranged along a phylogenetic tree of Archosauria.
Figure 2: Reconstructed body volumes.
Figure 3: Estimated evolutionary trends in whole-body CoM position along the craniocaudal axis.
Figure 4: Estimated evolutionary trends.
Figure 5: Estimated evolutionary trends for tail segment and M. caudofemoralis longus muscle masses.

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Acknowledgements

We thank the following people and institutions for access to fossil specimens: S. Chapman, A. Milner, P. Holroyd, M. Goodwin, K. Padian, M. Ryan, G. Jackson, D. Chapman, H.-J. Siber, B. Pabst, Z. Zhou and M. Norell; and the NHM (UK), UCMP (USA), CMNH (USA), IVPP (Canada); Sauriermuseum Aathal (Switzerland) and AMNH (USA). We wish to thank the following people, institutions and companies for providing digitized specimens, reconstructed specimens or both: O. Grillo, H. Mallison, J. Hertel, J. Brougham, M. Davis, J. A. Bannister; and the Universidade Federal do Rio de Janeiro (Brazil), MNB (Germany), Crescendo Games (Canada), NOVA/WGBH (USA) and Mechanimal (USA). We thank J. Molnar and RVC for invaluable assistance in processing computed tomography and laser-scan data, and for video editing. This work was supported by the following grants and institutions: NERC grant no. NE/G005877/1 to J.R.H., a Royal Society International Joint Project to J.R.H. and Z. Zhou (not a co-author), and the Sam and Doris Welles Fund (University of California) as part of PhD funding to V.A.

Author information

Authors and Affiliations

  1. Institut für Spezielle Zoologie und Evolutionsbiologie, Friedrich-Schiller-University Jena, 07743 Jena, Germany,

    Vivian Allen

  2. Structure & Motion Laboratory, The Royal Veterinary College, Hatfield, AL9 7TA, UK

    Vivian Allen & John R. Hutchinson

  3. Department of Musculoskeletal Biology II, Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool, L69 3GA, UK

    Karl T. Bates

  4. Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100034, China,

    Zhiheng Li

  5. Department of Geological Sciences, University of Texas at Austin, Austin, 78712-1692, Texas, USA

    Zhiheng Li

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Contributions

K.T.B., V.A. and Z.L. digitized fossil material. V.A. and K.T.B. constructed and analysed volumetric reconstructions. J.R.H. and V.A. performed phylogenetic optimization analysis. V.A. performed all statistical analyses. J.R.H. supervised and contributed ideas throughout the project. All authors contributed to the manuscript.

Corresponding author

Correspondence to John R. Hutchinson.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Text on text on evolutionary trends in morphological evolution, investigation of scaling and phylogenetic biases as well as alternate phylogenetic relationships, Supplementary References, Supplementary Figures 1-3 (including dorsoventral CoM changes and alternative phylogeny with analyses complementing Figures 1,3-5) and Supplementary Tables 1-12 that provide specimen information and data for all major inputs and outputs of our analyses. (PDF 956 kb)

Visualization of 3D modelling approach for extinct animal body dimensions

Reconstruction (flesh and air spaces) and iteration (minimum, maximum masses) methodology, using Allosaurus as an example. (MOV 12274 kb)

Rotating videos of all 17 archosaurs modelled and their relations to the main stem of archosaur phylogeny.

All 17 archosaurian models shown by proceeding in sequence along the phylogeny in Figure 1, showing specimens (with specimen numbers in brackets; see Supplementary Table S1) that are connected to nodes 1-16 as a means of visually conveying gross changes in body proportions along the bird-line. Note that the precise morphology of individual specimens is not ancestral at the nodes but is correlated with that ancestral morphology; see Figures 3-5 and Supplementary Information for details on ancestral morphology. (MOV 29309 kb)

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Allen, V., Bates, K., Li, Z. et al. Linking the evolution of body shape and locomotor biomechanics in bird-line archosaurs. Nature 497, 104–107 (2013). https://doi.org/10.1038/nature12059

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