A broad mutational target explains a fast rate of phenotypic evolution

  1. Fabrice Besnard  Is a corresponding author
  2. Joao Picao-Osorio
  3. Clément Dubois
  4. Marie-Anne Félix  Is a corresponding author
  1. INRA, France
  2. CNRS, France
  3. Universite de Recherche PSL, France

Abstract

The rapid evolution of a trait in a group of organisms can be explained by the sustained action of natural selection or by a high mutational variance, i.e. the propensity to change under spontaneous mutation. The causes for a high mutational variance are still elusive. In some cases, fast evolution depends on the high mutation rate of one or few loci with short tandem repeats. Here, we report on the fastest evolving cell fate among vulva precursor cells in Caenorhabditis nematodes, that of P3.p. We identify and validate causal mutations underlying P3.p's high mutational variance. We find that these positions do not present any characteristics of a high mutation rate, are scattered across the genome and the corresponding genes belong to distinct biological pathways. Our data indicate that a broad mutational target size is the cause of the high mutational variance and of the corresponding fast phenotypic evolutionary rate.

Data availability

Sequencing data have been deposited at EBI under accessions PRJEB30820-2. All other data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided in Suppl File 1.

The following data sets were generated

Article and author information

Author details

  1. Fabrice Besnard

    ENS, INRA, Paris, France
    For correspondence
    fabrice.besnard@ens-lyon.fr
    Competing interests
    The authors declare that no competing interests exist.
  2. Joao Picao-Osorio

    IBENS, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Clément Dubois

    IBENS, Universite de Recherche PSL, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Marie-Anne Félix

    IBENS, CNRS, Paris, France
    For correspondence
    felix@biologie.ens.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2635-3141

Funding

Agence Nationale de la Recherche (ANR-12-BSV2-0004-01)

  • Marie-Anne Félix

Agence Nationale de la Recherche (ANR-18-CE13-0006-01)

  • Marie-Anne Félix

Marie Sklodowska-Curie Training Grant (751530-EvoCellFate)

  • Joao Picao-Osorio

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: January 6, 2020
  2. Accepted: August 27, 2020
  3. Accepted Manuscript published: August 27, 2020 (version 1)
  4. Version of Record published: October 14, 2020 (version 2)

Copyright

© 2020, Besnard 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. Fabrice Besnard
  2. Joao Picao-Osorio
  3. Clément Dubois
  4. Marie-Anne Félix
(2020)
A broad mutational target explains a fast rate of phenotypic evolution
eLife 9:e54928.
https://doi.org/10.7554/eLife.54928
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