Adaptive evolution of nontransitive fitness in yeast

  1. Sean W Buskirk
  2. Alecia B Rokes
  3. Gregory I Lang  Is a corresponding author
  1. Lehigh University, United States

Abstract

A common misconception is that evolution is a linear 'march of progress', where each organism along a line of descent is more fit than all those that came before it. Rejecting this misconception implies that evolution is nontransitive: a series of adaptive events will, on occasion, produce organisms that are less fit compared to a distant ancestor. Here we identify a nontransitive evolutionary sequence in a 1,000-generation yeast evolution experiment. We show that nontransitivity arises due to adaptation in the yeast nuclear genome combined with the stepwise deterioration of an intracellular virus, which provides an advantage over viral competitors within host cells. Extending our analysis, we find that nearly half of our ~140 populations experience multilevel selection, fixing adaptive mutations in both the nuclear and viral genomes. Our results provide a mechanistic case-study for the adaptive evolution of nontransitivity due to multilevel selection in a 1,000-generation host/virus evolution experiment.

Data availability

Illumina data of viral competitions and evolved nuclear genomes are accessible under the BioProject ID PRJNA553562 and PRJNA205542, respectively.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Sean W Buskirk

    Biological Sciences, Lehigh University, Bethlehem, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1213-8130
  2. Alecia B Rokes

    Biological Sciences, Lehigh University, Bethlehem, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9496-0296
  3. Gregory I Lang

    Biological Sciences, Lehigh University, Bethlehem, United States
    For correspondence
    glang@lehigh.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7931-0428

Funding

National Institutes of Health (R01GM127420)

  • Gregory I Lang

Lehigh University (Faculty Innovation Grant)

  • Gregory I Lang

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

Reviewing Editor

  1. Wenying Shou, University College London, United Kingdom

Publication history

  1. Received: August 18, 2020
  2. Accepted: December 25, 2020
  3. Accepted Manuscript published: December 29, 2020 (version 1)
  4. Version of Record published: February 16, 2021 (version 2)

Copyright

© 2020, Buskirk 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. Sean W Buskirk
  2. Alecia B Rokes
  3. Gregory I Lang
(2020)
Adaptive evolution of nontransitive fitness in yeast
eLife 9:e62238.
https://doi.org/10.7554/eLife.62238
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