1. Evolutionary Biology
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Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation

  1. Grant Kinsler
  2. Kerry Geiler-Samerotte
  3. Dmitri A Petrov  Is a corresponding author
  1. Stanford University, United States
  2. Arizona State University, United States
Research Article
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Cite this article as: eLife 2020;9:e61271 doi: 10.7554/eLife.61271

Abstract

Building a genotype-phenotype-fitness map of adaptation is a central goal in evolutionary biology. It is difficult even when adaptive mutations are known because it is hard to enumerate which phenotypes make these mutations adaptive. We address this problem by first quantifying how the fitness of hundreds of adaptive yeast mutants responds to subtle environmental shifts. We then model the number of phenotypes these mutations collectively influence by decomposing these patterns of fitness variation. We find that a small number of inferred phenotypes can predict fitness of the adaptive mutations near their original glucose-limited evolution condition. Importantly, inferred phenotypes that matter little to fitness at or near the evolution condition can matter strongly in distant environments. This suggests that adaptive mutations are locally modular—affecting a small number of phenotypes that matter to fitness in the environment where they evolved—yet globally pleiotropic—affecting additional phenotypes that may reduce or improve fitness in new environments.

Article and author information

Author details

  1. Grant Kinsler

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8308-4665
  2. Kerry Geiler-Samerotte

    Biodesign Institute, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4666-2192
  3. Dmitri A Petrov

    Department of Biology, Stanford University, Stanford, United States
    For correspondence
    dpetrov@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3664-9130

Funding

National Institutes of Health (R35GM118165)

  • Dmitri A Petrov

National Institutes of Health (R35GM133674)

  • Kerry Geiler-Samerotte

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Vaughn S Cooper, University of Pittsburgh, United States

Publication history

  1. Received: July 20, 2020
  2. Accepted: December 2, 2020
  3. Accepted Manuscript published: December 2, 2020 (version 1)

Copyright

© 2020, Kinsler 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.

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