Strong biomechanical relationships bias the tempo and mode of morphological evolution

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Abstract

The influence of biomechanics on the tempo and mode of morphological evolution is unresolved, yet is fundamental to organismal diversification. Across multiple four-bar linkage systems in animals, we discovered that rapid morphological evolution (tempo) is associated with mechanical sensitivity (strong correlation between a mechanical system's output and one or more of its components). Mechanical sensitivity is explained by size: the smallest link(s) are disproportionately affected by length changes and most strongly influence mechanical output. Rate of evolutionary change (tempo) is greatest in the smallest links and trait shifts across phylogeny (mode) occur exclusively via the influential, small links. Our findings illuminate the paradigms of many-to-one mapping, mechanical sensitivity, and constraints: tempo and mode are dominated by strong correlations that exemplify mechanical sensitivity, even in linkage systems known for exhibiting many-to-one mapping. Amidst myriad influences, mechanical sensitivity imparts distinct, predictable footprints on morphological diversity.

Data availability

All datasets and phylogenies are included in full in the supplementary materials. Citations to the original papers containing these datasets and phylogenies are included with the supplementary files.

Article and author information

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Martha M Muñoz

Department of Biological Sciences, Virginia Tech, Blacksburg, United States

For correspondence
mmunoz5@vt.edu

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

Department of Biological Sciences, University of Rhode Island, Kingston, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9304-519X
Philip SL Anderson

Department of Animal Biology, University of Illinois, Urbana Champaign, Urbana, United States

Competing interests
The authors declare that no competing interests exist.
S N Patek

Department of Biology, Duke University, Durham, United States

For correspondence
snp2@duke.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9738-882X

Funding

National Science Foundation (1439850)

S N Patek

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.