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

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 timin...

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Main Authors: Priscila S Rothier, Anne-Claire Fabre, Julien Clavel, Roger BJ Benson, Anthony Herrel
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/81492
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author Priscila S Rothier
Anne-Claire Fabre
Julien Clavel
Roger BJ Benson
Anthony Herrel
author_facet Priscila S Rothier
Anne-Claire Fabre
Julien Clavel
Roger BJ Benson
Anthony Herrel
author_sort Priscila S Rothier
collection DOAJ
description 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.
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spelling doaj.art-59345325008844a88b4d47b0fefbea0b2023-02-08T14:53:15ZengeLife Sciences Publications LtdeLife2050-084X2023-01-011210.7554/eLife.81492Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversityPriscila S Rothier0https://orcid.org/0000-0003-3017-6528Anne-Claire Fabre1Julien Clavel2Roger BJ Benson3Anthony Herrel4Département Adaptations du Vivant, Muséum National d'Histoire Naturelle, Paris, FranceNaturhistorisches Museum Bern, Bern, Switzerland; Institute of Ecology and Evolution, University of Bern, Bern, Switzerland; Life Sciences Department, Vertebrates Division, Natural History Museum, London, United KingdomLife Sciences Department, Vertebrates Division, Natural History Museum, London, United Kingdom; Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023, Villeurbanne, FranceDepartment of Earth Sciences, University of Oxford, Oxford, United KingdomDépartement Adaptations du Vivant, Muséum National d'Histoire Naturelle, Paris, FranceVertebrate 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.https://elifesciences.org/articles/81492mammaliamarsupialiamonotremataplacentalia
spellingShingle Priscila S Rothier
Anne-Claire Fabre
Julien Clavel
Roger BJ Benson
Anthony Herrel
Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity
eLife
mammalia
marsupialia
monotremata
placentalia
title Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity
title_full Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity
title_fullStr Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity
title_full_unstemmed Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity
title_short Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity
title_sort mammalian forelimb evolution is driven by uneven proximal to distal morphological diversity
topic mammalia
marsupialia
monotremata
placentalia
url https://elifesciences.org/articles/81492
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AT anneclairefabre mammalianforelimbevolutionisdrivenbyunevenproximaltodistalmorphologicaldiversity
AT julienclavel mammalianforelimbevolutionisdrivenbyunevenproximaltodistalmorphologicaldiversity
AT rogerbjbenson mammalianforelimbevolutionisdrivenbyunevenproximaltodistalmorphologicaldiversity
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