Pleiotropic mutations can rapidly evolve to directly benefit self and cooperative partner despite unfavorable conditions

  1. Samuel Frederick Mock Hart
  2. Chi-Chun Chen
  3. Wenying Shou  Is a corresponding author
  1. Fred Hutchinson Cancer Research Center, United States
  2. University College London, United Kingdom

Abstract

Cooperation, paying a cost to benefit others, is widespread. Cooperation can be promoted by pleiotropic 'win-win' mutations which directly benefit self ('self-serving') and partner ('partner-serving'). Previously, we showed that partner-serving should be defined as increased benefit supply rate per intake benefit (Hart & Pineda et al., 2019). Here, we report that win-win mutations can rapidly evolve even under conditions unfavorable for cooperation. Specifically, in a well-mixed environment we evolved engineered yeast cooperative communities where two strains exchanged costly metabolites lysine and hypoxanthine. Among cells that consumed lysine and released hypoxanthine, ecm21 mutations repeatedly arose. ecm21 is self-serving, improving self's growth rate in limiting lysine. ecm21 is also partner-serving, increasing hypoxanthine release rate per lysine consumption and the steady state growth rate of partner. ecm21 also arose in monocultures evolving in lysine-limited chemostats. Thus, even without any history of cooperation or pressure to maintain cooperation, pleiotropic win-win mutations may readily evolve.

Data availability

All data in this study are included in the manuscript and supporting files. Source data files have been provided for Figures 2-4.

Article and author information

Author details

  1. Samuel Frederick Mock Hart

    Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5068-2199
  2. Chi-Chun Chen

    Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Wenying Shou

    Genetics, Evolution and Environment, University College London, London, United Kingdom
    For correspondence
    w.shou@ucl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5693-381X

Funding

National Institutes of Health (DP2 OD006498-01)

  • Samuel Frederick Mock Hart
  • Chi-Chun Chen
  • Wenying Shou

National Institutes of Health (R01GM124128)

  • Samuel Frederick Mock Hart
  • Wenying Shou

W.M. Keck Foundation (Distinguished Young Scholars)

  • Chi-Chun Chen
  • Wenying Shou

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

Reviewing Editor

  1. Kevin J Verstrepen, VIB-KU Leuven Center for Microbiology, Belgium

Version history

  1. Received: April 20, 2020
  2. Accepted: January 26, 2021
  3. Accepted Manuscript published: January 27, 2021 (version 1)
  4. Version of Record published: June 7, 2021 (version 2)

Copyright

© 2021, Hart 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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  1. Samuel Frederick Mock Hart
  2. Chi-Chun Chen
  3. Wenying Shou
(2021)
Pleiotropic mutations can rapidly evolve to directly benefit self and cooperative partner despite unfavorable conditions
eLife 10:e57838.
https://doi.org/10.7554/eLife.57838

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https://doi.org/10.7554/eLife.57838

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