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

Version 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.

Metrics

  • 3,787
    views
  • 466
    downloads
  • 23
    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. 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

Share this article

https://doi.org/10.7554/eLife.62238

Further reading

    1. Biochemistry and Chemical Biology
    2. Evolutionary Biology
    Foteini Karapanagioti, Úlfur Águst Atlason ... Sebastian Obermaier
    Research Article

    The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Yannick Schäfer, Katja Palitzsch ... Jaanus Suurväli
    Research Article Updated

    Copy number variation in large gene families is well characterized for plant resistance genes, but similar studies are rare in animals. The zebrafish (Danio rerio) has hundreds of NLR immune genes, making this species ideal for studying this phenomenon. By sequencing 93 zebrafish from multiple wild and laboratory populations, we identified a total of 1513 NLRs, many more than the previously known 400. Approximately half of those are present in all wild populations, but only 4% were found in 80% or more of the individual fish. Wild fish have up to two times as many NLRs per individual and up to four times as many NLRs per population than laboratory strains. In contrast to the massive variability of gene copies, nucleotide diversity in zebrafish NLR genes is very low: around half of the copies are monomorphic and the remaining ones have very few polymorphisms, likely a signature of purifying selection.