1. Evolutionary Biology
  2. Genetics and Genomics
Download icon

The distribution of fitness effects among synonymous mutations in a gene under directional selection

  1. Eleonore Lebeuf-Taylor
  2. Nick McCloskey
  3. Susan F Bailey
  4. Aaron Hinz
  5. Rees Kassen  Is a corresponding author
  1. University of Ottawa, Canada
  2. Clarkson University, United States
Research Article
  • Cited 0
  • Views 1,476
  • Annotations
Cite this article as: eLife 2019;8:e45952 doi: 10.7554/eLife.45952

Abstract

The fitness effects of synonymous mutations, nucleotide changes that do not alter the encoded amino acid, have often been assumed to be neutral, but a growing body of evidence suggests otherwise. We used site-directed mutagenesis coupled with direct measures of competitive fitness to estimate the distribution of fitness effects among synonymous mutations for a gene under directional selection and capable of adapting via synonymous nucleotide changes. Synonymous mutations had highly variable fitness effects, both deleterious and beneficial, resembling those of nonsynonymous mutations in the same gene. This variation in fitness was underlain by changes in transcription linked to the creation of internal promoter sites. A positive correlation between fitness and the presence of synonymous substitutions across a phylogeny of related Pseudomonads suggests these mutations may be common in nature. Taken together, our results provide the most compelling evidence to date that synonymous mutations with non-neutral fitness effects may in fact be commonplace.

Article and author information

Author details

  1. Eleonore Lebeuf-Taylor

    Department of Biology, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Nick McCloskey

    Department of Biology, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Susan F Bailey

    Department of Biology, Clarkson University, Potsdam, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2294-1229
  4. Aaron Hinz

    Department of Biology, University of Ottawa, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Rees Kassen

    Department of Biology, University of Ottawa, Ottawa, Canada
    For correspondence
    rees.kassen@uottawa.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5617-4259

Funding

Natural Sciences and Engineering Research Council of Canada (Discovery Grant)

  • Rees Kassen

Natural Sciences and Engineering Research Council of Canada (Canada Graduate Scholarship)

  • Eleonore Lebeuf-Taylor

Ontario Ministry of Economic Development and Innovation (Ontario Graduate Scholarship)

  • Nick McCloskey

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

Reviewing Editor

  1. Christian R Landry, Université Laval, Canada

Publication history

  1. Received: February 10, 2019
  2. Accepted: July 18, 2019
  3. Accepted Manuscript published: July 19, 2019 (version 1)
  4. Version of Record published: August 13, 2019 (version 2)

Copyright

© 2019, Lebeuf-Taylor 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

  • 1,476
    Page views
  • 234
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Evolutionary Biology
    2. Microbiology and Infectious Disease
    Jan Janouškovec et al.
    Research Article
    1. Evolutionary Biology
    2. Genetics and Genomics
    Evan Witt et al.
    Research Article