Strong biomechanical relationships bias the tempo and mode of morphological evolution

  1. Martha M Muñoz  Is a corresponding author
  2. Yinan Hu
  3. Philip SL Anderson
  4. S N Patek  Is a corresponding author
  1. Virginia Tech, United States
  2. University of Rhode Island, United States
  3. University of Illinois, Urbana Champaign, United States
  4. Duke University, United States

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

Author details

  1. 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.
  2. Yinan Hu

    Department of Biological Sciences, University of Rhode Island, Kingston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9304-519X
  3. 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.
  4. 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.
    ORCID icon "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

© 2018, Muñoz 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.

Metrics

  • 2,461
    views
  • 339
    downloads
  • 43
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Martha M Muñoz
  2. Yinan Hu
  3. Philip SL Anderson
  4. S N Patek
(2018)
Strong biomechanical relationships bias the tempo and mode of morphological evolution
eLife 7:e37621.
https://doi.org/10.7554/eLife.37621

Share this article

https://doi.org/10.7554/eLife.37621

Further reading

    1. Ecology
    Ming-Qiang Wang, Shi-Kun Guo ... Chao-Dong Zhu
    Research Article

    Environmental factors can influence ecological networks, but these effects are poorly understood in the realm of the phylogeny of host-parasitoid interactions. Especially, we lack a comprehensive understanding of the ways that biotic factors, including plant species richness, overall community phylogenetic and functional composition of consumers, and abiotic factors such as microclimate, determine host-parasitoid network structure and host-parasitoid community dynamics. To address this, we leveraged a 5-year dataset of trap-nesting bees and wasps and their parasitoids collected in a highly controlled, large-scale subtropical tree biodiversity experiment. We tested for effects of tree species richness, tree phylogenetic, and functional diversity, and species and phylogenetic composition on species and phylogenetic diversity of both host and parasitoid communities and the composition of their interaction networks. We show that multiple components of tree diversity and canopy cover impacted both, species and phylogenetic composition of hosts and parasitoids. Generally, phylogenetic associations between hosts and parasitoids reflected nonrandomly structured interactions between phylogenetic trees of hosts and parasitoids. Further, host-parasitoid network structure was influenced by tree species richness, tree phylogenetic diversity, and canopy cover. Our study indicates that the composition of higher trophic levels and corresponding interaction networks are determined by plant diversity and canopy cover, especially via trophic links in species-rich ecosystems.

    1. Ecology
    Itai Bloch, David Troupin ... Nir Sapir
    Research Article

    Optimal foraging theory posits that foragers adjust their movements based on prey abundance to optimize food intake. While extensively studied in terrestrial and marine environments, aerial foraging has remained relatively unexplored due to technological limitations. This study, uniquely combining BirdScan-MR1 radar and the Advanced Tracking and Localization of Animals in Real-Life Systems biotelemetry system, investigates the foraging dynamics of Little Swifts (Apus affinis) in response to insect movements over Israel’s Hula Valley. Insect movement traffic rate (MoTR) substantially varied across days, strongly influencing swift movement. On days with high MoTR, swifts exhibited reduced flight distance, increased colony visit rate, and earlier arrivals at the breeding colony, reflecting a dynamic response to prey availability. However, no significant effects were observed in total foraging duration, flight speed, or daily route length. Notably, as insect abundance increased, inter-individual distances decreased. These findings suggest that Little Swifts optimize their foraging behavior in relation to aerial insect abundance, likely influencing reproductive success and population dynamics. The integration of radar technology and biotelemetry systems provides a unique perspective on the interactions between aerial insectivores and their prey, contributing to a comprehensive understanding of optimal foraging strategies in diverse environments.