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

  • 2,481
    views
  • 342
    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
    2. Evolutionary Biology
    Vendula Bohlen Šlechtová, Tomáš Dvořák ... Joerg Bohlen
    Research Article

    Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.

    1. Ecology
    2. Neuroscience
    Kathleen T Quach, Gillian A Hughes, Sreekanth H Chalasani
    Research Article

    Prey must balance predator avoidance with feeding, a central dilemma in prey refuge theory. Additionally, prey must assess predatory imminence—how close threats are in space and time. Predatory imminence theory classifies defensive behaviors into three defense modes: pre-encounter, post-encounter, and circa-strike, corresponding to increasing levels of threat—–suspecting, detecting, and contacting a predator. Although predatory risk often varies in spatial distribution and imminence, how these factors intersect to influence defensive behaviors is poorly understood. Integrating these factors into a naturalistic environment enables comprehensive analysis of multiple defense modes in consistent conditions. Here, we combine prey refuge and predatory imminence theories to develop a model system of nematode defensive behaviors, with Caenorhabditis elegans as prey and Pristionchus pacificus as predator. In a foraging environment comprised of a food-rich, high-risk patch and a food-poor, low-risk refuge, C. elegans innately exhibits circa-strike behaviors. With experience, it learns post- and pre-encounter behaviors that proactively anticipate threats. These defense modes intensify with predator lethality, with only life-threatening predators capable of eliciting all three modes. SEB-3 receptors and NLP-49 peptides, key stress regulators, vary in their impact and interdependence across defense modes. Overall, our model system reveals fine-grained insights into how stress-related signaling regulates defensive behaviors.