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

Abstract
Data availability
Article and author information
Metrics

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

1. Rothier PS
2. Fabre A
3. Clavel J
4. Benson R
5. Herrel A
(2023) Input data from: Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity
Dryad Digital Repository, doi:10.5061/dryad.0cfxpnw6h.

https://dx.doi.org/10.5061/dryad.0cfxpnw6h

The following previously published data sets were used

(2019) Inferring the mammal tree: Species-level sets of phylogenies for questions in ecology, evolution, and conservation
Dryad Digital Repository, doi:10.5061/dryad.tb03d03.

https://dx.doi.org/10.5061/dryad.tb03d03

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0003-3017-6528
Anne-Claire Fabre

Naturhistorisches Museum Bern, Bern, Switzerland

Competing interests
The authors declare that no competing interests exist.
Julien Clavel

Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023, Villeurbanne, France

Competing interests
The authors declare that no competing interests exist.
Roger BJ Benson

Department of Earth Sciences, University of Oxford, Oxford, United Kingdom

Competing interests
The authors declare that no competing interests exist.
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.

Copyright

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.