Evolution of haploid and diploid populations reveals common, strong, and variable pleiotropic effects in non-home environments

Abstract

Adaptation is driven by the selection for beneficial mutations that provide a fitness advantage in the specific environment in which a population is evolving. However, environments are rarely constant or predictable. When an organism well adapted to one environment finds itself in another, pleiotropic effects of mutations that made it well adapted to its former environment will affect its success. To better understand such pleiotropic effects, we evolved both haploid and diploid barcoded budding yeast populations in multiple environments, isolated adaptive clones, and then determined the fitness effects of adaptive mutations in “non-home” environments in which they were not selected. We find that pleiotropy is common, with most adaptive evolved lineages showing fitness effects in non-home environments. Consistent with other studies, we find that these pleiotropic effects are unpredictable: they are beneficial in some environments and deleterious in others. However, we do find that lineages with adaptive mutations in the same genes tend to show similar pleiotropic effects. We also find that ploidy influences the observed adaptive mutational spectra in a condition-specific fashion. In some conditions, haploids and diploids are selected with adaptive mutations in identical genes, while in others they accumulate mutations in almost completely disjoint sets of genes.

Data availability

All underlying sequencing data for both barcode sequencing and whole genome sequencing are available from the short read archive (SRA) under accession number PRJNA912754.

The following data sets were generated

Article and author information

Author details

  1. Vivian Chen

    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:" 0009-0007-6205-7853
  2. Milo S Johnson

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0169-2494
  3. Lucas Hérissant

    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:" 0000-0003-0065-5608
  4. Parris T Humphrey

    Department of Organismic and Evolutionary Biology, Harvard University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David C Yuan

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Yuping Li

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Atish Agarwala

    Department of Physics, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Samuel B Hoelscher

    Department of Genetics, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Dmitri A Petrov

    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:" 0000-0002-3664-9130
  10. Michael M Desai

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9581-1150
  11. Gavin Sherlock

    Department of Genetics, Stanford University, Stanford, United States
    For correspondence
    gsherloc@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1692-4983

Funding

National Institute of General Medical Sciences (R35 GM131824)

  • Gavin Sherlock

National Institute of General Medical Sciences (R35 GM118165)

  • Dmitri A Petrov

National Institute of General Medical Sciences (R01 GM104239)

  • Michael M Desai

National Science Foundation (PHY-1914916)

  • Michael M Desai

National Science Foundation (DMS-1764269)

  • Michael M Desai

National Science Foundation

  • Milo S Johnson

National Institute of General Medical Sciences (R01 GM110275)

  • Gavin Sherlock

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

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Biology Tübingen, Germany

Version history

  1. Preprint posted: March 1, 2023 (view preprint)
  2. Received: September 21, 2023
  3. Accepted: September 27, 2023
  4. Accepted Manuscript published: October 20, 2023 (version 1)
  5. Version of Record published: November 7, 2023 (version 2)
  6. Version of Record updated: November 8, 2023 (version 3)

Copyright

© 2023, Chen 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. Vivian Chen
  2. Milo S Johnson
  3. Lucas Hérissant
  4. Parris T Humphrey
  5. David C Yuan
  6. Yuping Li
  7. Atish Agarwala
  8. Samuel B Hoelscher
  9. Dmitri A Petrov
  10. Michael M Desai
  11. Gavin Sherlock
(2023)
Evolution of haploid and diploid populations reveals common, strong, and variable pleiotropic effects in non-home environments
eLife 12:e92899.
https://doi.org/10.7554/eLife.92899

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https://doi.org/10.7554/eLife.92899

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