A toxin-antidote selfish element increases fitness of its host

  1. Lijiang Long
  2. Wen Xu
  3. Francisco Valencia
  4. Annalise B Paaby  Is a corresponding author
  5. Patrick T McGrath  Is a corresponding author
  1. Georgia Institute of Technology, United States

Abstract

Selfish genetic elements can promote their transmission at the expense of individual survival, creating conflict between the element and the rest of the genome. Recently, a large number of toxin-antidote (TA) post-segregation distorters have been identified in non-obligate outcrossing nematodes. Their origin and the evolutionary forces that keep them at intermediate population frequencies are poorly understood. Here, we study a TA element in C. elegans called zeel-1;peel-1. Two major haplotypes of this locus, with and without the selfish element, segregate in C. elegans. We evaluate the fitness consequences of the zeel-1;peel-1 element outside of its role in gene drive in non-outcrossing animals, and demonstrate that loss of the toxin peel-1 decreased fitness of hermaphrodites and resulted in reductions in fecundity and body size. These findings suggest a biological role for peel-1 beyond toxin lethality. This work demonstrates that a TA element can provide a fitness benefit to its hosts, either during their initial evolution or by being co-opted by the animals following their selfish spread. These findings guide our understanding on how TA elements can remain in a population where gene drive is minimized, helping resolve the mystery of prevalent TA elements in selfing animals.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for all figures . Simulation code is included in a github: https://github.com/lijiang-long/TA_modeling.

Article and author information

Author details

  1. Lijiang Long

    School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9897-5900
  2. Wen Xu

    School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2085-7223
  3. Francisco Valencia

    School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Annalise B Paaby

    School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    For correspondence
    paaby@gatech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1422-047X
  5. Patrick T McGrath

    School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    For correspondence
    patrick.mcgrath@biology.gatech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1598-3746

Funding

National Institutes of Health (GM139594)

  • Patrick T McGrath

National Institutes of Health (GM119744)

  • Annalise B Paaby

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

Reviewing Editor

  1. Erik C Andersen, Northwestern University, United States

Version history

  1. Received: July 5, 2022
  2. Preprint posted: July 15, 2022 (view preprint)
  3. Accepted: October 23, 2023
  4. Accepted Manuscript published: October 24, 2023 (version 1)
  5. Version of Record published: November 7, 2023 (version 2)

Copyright

© 2023, Long 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. Lijiang Long
  2. Wen Xu
  3. Francisco Valencia
  4. Annalise B Paaby
  5. Patrick T McGrath
(2023)
A toxin-antidote selfish element increases fitness of its host
eLife 12:e81640.
https://doi.org/10.7554/eLife.81640

Share this article

https://doi.org/10.7554/eLife.81640

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