Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity

  1. Priscila S Rothier  Is a corresponding author
  2. Anne-Claire Fabre
  3. Julien Clavel
  4. Roger BJ Benson
  5. Anthony Herrel
  1. Muséum National d'Histoire Naturelle, France
  2. Naturhistorisches Museum Bern, Switzerland
  3. Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023, France
  4. University of Oxford, United Kingdom

Abstract

Vertebrate limb morphology often reflects the environment due to variation in locomotor requirements. However, proximal and distal limb segments may evolve differently from one another, reflecting an anatomical gradient of functional specialization that has been suggested to be impacted by the timing of development. Here we explore whether the temporal sequence of bone condensation predicts variation in the capacity of evolution to generate morphological diversity in proximal and distal forelimb segments across more than 600 species of mammals. Distal elements not only exhibit greater shape diversity, but also show stronger within-element integration and, on average, faster evolutionary responses than intermediate and upper limb segments. Results are consistent with the hypothesis that late developing distal bones display greater morphological variation than more proximal limb elements. However, the higher integration observed within the autopod deviates from such developmental predictions, suggesting that functional specialization plays an important role in driving within-element covariation. Proximal and distal limb segments also show different macroevolutionary patterns, albeit not showing a perfect proximo-distal gradient. The high disparity of the mammalian autopod, reported here, is consistent with the higher potential of development to generate variation in more distal limb structures, as well as functional specialization of the distal elements.

Data availability

Morphometric data and R codes are available on Dryad (DOI: 10.5061/dryad.0cfxpnw6h)

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Priscila S Rothier

    Département Adaptations du Vivant, Muséum National d'Histoire Naturelle, Paris, France
    For correspondence
    priscilasrd@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3017-6528
  2. Anne-Claire Fabre

    Naturhistorisches Museum Bern, Bern, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Julien Clavel

    Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023, Villeurbanne, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Roger BJ Benson

    Department of Earth Sciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Anthony Herrel

    Département Adaptations du Vivant, Muséum National d'Histoire Naturelle, Paris, France
    Competing interests
    The authors declare that no competing interests exist.

Funding

Conselho Nacional de Desenvolvimento Científico e Tecnológico (204841/2018-6)

  • Priscila S Rothier

European Research Council (2015-STG-677774)

  • Roger BJ Benson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Marianne E Bronner, California Institute of Technology, United States

Version history

  1. Received: June 29, 2022
  2. Preprint posted: July 28, 2022 (view preprint)
  3. Accepted: January 24, 2023
  4. Accepted Manuscript published: January 26, 2023 (version 1)
  5. Version of Record published: February 8, 2023 (version 2)

Copyright

© 2023, Rothier et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Priscila S Rothier
  2. Anne-Claire Fabre
  3. Julien Clavel
  4. Roger BJ Benson
  5. Anthony Herrel
(2023)
Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity
eLife 12:e81492.
https://doi.org/10.7554/eLife.81492

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https://doi.org/10.7554/eLife.81492