Selfing is the safest sex for Caenorhabditis tropicalis

  1. Luke M Noble  Is a corresponding author
  2. John Yuen
  3. Lewis Stevens
  4. Nicolas D Moya
  5. Riaad Persaud
  6. Marc Moscatelli
  7. Jacqueline L Jackson
  8. Gaotian Zhang
  9. Rojin Chitrakar
  10. L Ryan Baugh
  11. Christian Braendle
  12. Erik C Andersen
  13. Hannah S Seidel
  14. Matthew V Rockman
  1. Ecole Normale Superieure, France
  2. New York University, United States
  3. Northwestern University, United States
  4. Duke University, United States
  5. Université Côte d'Azur, CNRS, Inserm, France
  6. Eastern Michigan University, United States

Abstract

Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, C. tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple Medea-like elements, genetically consistent with maternal toxin/zygotic antidote systems. Loci with Medea activity harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating Medea elements dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid Medea-mediated outbreeding depression.

Data availability

All sequencing reads used in this project are available from the NCBI Sequence Read Archive under accession PRJNA662844. Software code is available from https://github.com/lukemn/tropicalis. All data generated or analysed during this study are included in the manuscript and supporting files. Source data and supplementary files have been provided for Figures 1,2,3,4,5,6,7,9,10,11,12.

The following data sets were generated

Article and author information

Author details

  1. Luke M Noble

    Institut de Biologie de l'ENS, Ecole Normale Superieure, Paris, France
    For correspondence
    noble@biologie.ens.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5161-4059
  2. John Yuen

    Department of Biology and Center for Genomics & Systems Biology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1569-3298
  3. Lewis Stevens

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6075-8273
  4. Nicolas D Moya

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6817-1784
  5. Riaad Persaud

    Department of Biology and Center for Genomics & Systems Biology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Marc Moscatelli

    Department of Biology and Center for Genomics & Systems Biology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jacqueline L Jackson

    Department of Biology and Center for Genomics & Systems Biology, New York University, Jersey City, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5376-0968
  8. Gaotian Zhang

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Rojin Chitrakar

    Department of Biology, Duke Center for Genomic and Computational Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. L Ryan Baugh

    Department of Biology, Duke Center for Genomic and Computational Biology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2148-5492
  11. Christian Braendle

    Institut de Biologie Valrose, Université Côte d'Azur, CNRS, Inserm, Nice, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Erik C Andersen

    Department of Molecular Biosciences, Northwestern University, Evanston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0229-9651
  13. Hannah S Seidel

    Department of Biology, Eastern Michigan University, Ypsilanti, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Matthew V Rockman

    Department of Biology and Center for Genomics & Systems Biology, New York University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6492-8906

Funding

National Institute of Environmental Health Sciences (ES029930)

  • Erik C Andersen

National Institute of Environmental Health Sciences (ES029930)

  • Matthew V Rockman

National Institute of General Medical Sciences (GM089972)

  • Matthew V Rockman

National Institute of General Medical Sciences (GM121828)

  • Matthew V Rockman

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

Reviewing Editor

  1. Vincent Castric, Université de Lille, France

Version history

  1. Received: August 29, 2020
  2. Accepted: January 8, 2021
  3. Accepted Manuscript published: January 11, 2021 (version 1)
  4. Version of Record published: February 1, 2021 (version 2)

Copyright

© 2021, Noble 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. Luke M Noble
  2. John Yuen
  3. Lewis Stevens
  4. Nicolas D Moya
  5. Riaad Persaud
  6. Marc Moscatelli
  7. Jacqueline L Jackson
  8. Gaotian Zhang
  9. Rojin Chitrakar
  10. L Ryan Baugh
  11. Christian Braendle
  12. Erik C Andersen
  13. Hannah S Seidel
  14. Matthew V Rockman
(2021)
Selfing is the safest sex for Caenorhabditis tropicalis
eLife 10:e62587.
https://doi.org/10.7554/eLife.62587

Share this article

https://doi.org/10.7554/eLife.62587

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