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.

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.

Metrics

  • 1,524
    views
  • 195
    downloads
  • 12
    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. 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

Share this article

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

Further reading

    1. Ecology
    2. Microbiology and Infectious Disease
    Tom Clegg, Samraat Pawar
    Research Article

    Predicting how species diversity changes along environmental gradients is an enduring problem in ecology. In microbes current theories tend to invoke energy availability and enzyme kinetics as the main drivers of temperature-richness relationships. Here we derive a general empirically-grounded theory that can explain this phenomenon by linking microbial species richness in competitive communities to variation in the temperature-dependence of their interaction and growth rates. Specifically, the shape of the microbial community temperature-richness relationship depends on how rapidly the strength of effective competition between species pairs changes with temperature relative to the variance of their growth rates. Furthermore, it predicts that a thermal specialist-generalist tradeoff in growth rates alters coexistence by shifting this balance, causing richness to peak at relatively higher temperatures. Finally, we show that the observed patterns of variation in thermal performance curves of metabolic traits across extant bacterial taxa is indeed sufficient to generate the variety of community-level temperature-richness responses observed in the real world. Our results provide a new and general mechanism that can help explain temperature-diversity gradients in microbial communities, and provide a quantitative framework for interlinking variation in the thermal physiology of microbial species to their community-level diversity.

    1. Ecology
    Chao Wen, Yuyi Lu ... Lars Chittka
    Research Article

    Bumblebees (Bombus terrestris) have been shown to engage in string-pulling behavior to access rewards. The objective of this study was to elucidate whether bumblebees display means-end comprehension in a string-pulling task. We presented bumblebees with two options: one where a string was connected to an artificial flower containing a reward and the other presenting an interrupted string. Bumblebees displayed a consistent preference for pulling connected strings over interrupted ones after training with a stepwise pulling technique. When exposed to novel string colors, bees continued to exhibit a bias towards pulling the connected string. This suggests that bumblebees engage in featural generalization of the visual display of the string connected to the flower in this task. If the view of the string connected to the flower was restricted during the training phase, the proportion of bumblebees choosing the connected strings significantly decreased. Similarly, when the bumblebees were confronted with coiled connected strings during the testing phase, they failed to identify and reject the interrupted strings. This finding underscores the significance of visual consistency in enabling the bumblebees to perform the task successfully. Our results suggest that bumblebees’ ability to distinguish between continuous strings and interrupted strings relies on a combination of image matching and associative learning, rather than means-end understanding. These insights contribute to a deeper understanding of the cognitive processes employed by bumblebees when tackling complex spatial tasks.