Mutational robustness changes during long-term adaptation in laboratory budding yeast populations

  1. Milo S Johnson  Is a corresponding author
  2. Michael M Desai  Is a corresponding author
  1. Harvard University, United States

Abstract

As an adapting population traverses the fitness landscape, its local neighborhood (i.e., the collection of fitness effects of single-step mutations) can change shape because of interactions with mutations acquired during evolution. These changes to the distribution of fitness effects can affect both the rate of adaptation and the accumulation of deleterious mutations. However, while numerous models of fitness landscapes have been proposed in the literature, empirical data on how this distribution changes during evolution remains limited. In this study, we directly measure how the fitness landscape neighborhood changes during laboratory adaptation. Using a barcode-based mutagenesis system, we measure the fitness effects of 91 specific gene disruption mutations in genetic backgrounds spanning 8,000-10,000 generations of evolution in two constant environments. We find that the mean of the distribution of fitness effects decreases in one environment, indicating a reduction in mutational robustness, but does not change in the other. We show that these distribution-level patterns result from differences in the relative frequency of certain patterns of epistasis at the level of individual mutations, including fitness-correlated and idiosyncratic epistasis.

Data availability

Raw sequencing data has been deposited in the GenBank SRA (accession: SRP351176). All code used in this project is available on GitHub (https://github.com/mjohnson11/VTn_pipeline). All figures are based on data included in Supplementary File 1.

The following data sets were generated

Article and author information

Author details

  1. Milo S Johnson

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    For correspondence
    milo.s.johnson.13@gmail.com
    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
  2. Michael M Desai

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    For correspondence
    mdesai@oeb.harvard.edu
    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

Funding

National Science Foundation (Graduate Research Fellowship)

  • Milo S Johnson

National Science Foundation (PHY-1914916)

  • Michael M Desai

National Institutes of Health (GM104239)

  • Michael M Desai

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: December 17, 2021
  2. Preprint posted: December 20, 2021 (view preprint)
  3. Accepted: July 25, 2022
  4. Accepted Manuscript published: July 26, 2022 (version 1)
  5. Version of Record published: August 5, 2022 (version 2)

Copyright

© 2022, Johnson & Desai

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. Milo S Johnson
  2. Michael M Desai
(2022)
Mutational robustness changes during long-term adaptation in laboratory budding yeast populations
eLife 11:e76491.
https://doi.org/10.7554/eLife.76491

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