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...
Main Authors: | , , , , |
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Format: | Article |
Language: | English |
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eLife Sciences Publications Ltd
2023-01-01
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Series: | eLife |
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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. |
first_indexed | 2024-04-10T16:34:29Z |
format | Article |
id | doaj.art-59345325008844a88b4d47b0fefbea0b |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-10T16:34:29Z |
publishDate | 2023-01-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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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