1. Evolutionary Biology
  2. Genetics and Genomics
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Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes

  1. Lauren N Booth
  2. Travis J Maures
  3. Robin W Yeo
  4. Cindy Tantilert
  5. Anne Brunet  Is a corresponding author
  1. Stanford University, United States
Research Article
  • Cited 6
  • Views 2,339
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Cite this article as: eLife 2019;8:e46418 doi: 10.7554/eLife.46418

Abstract

Sexual interactions have a potent influence on health in several species, including mammals. Previous work in C. elegans identified strategies used by males to accelerate the demise of the opposite sex (hermaphrodites). But whether hermaphrodites evolved counter-strategies against males remains unknown. Here we discover that young C. elegans hermaphrodites are remarkably resistant to brief sexual encounters with males, whereas older hermaphrodites succumb prematurely. Surprisingly, it is not their youthfulness that protects young hermaphrodites, but the fact that they have self-sperm. The beneficial effect of self-sperm is mediated by a sperm-sensing pathway acting on the soma rather than by fertilization. Activation of this pathway in females triggers protection from the negative impact of males. Interestingly, the role of self-sperm in protecting against the detrimental effects of males evolved independently in hermaphroditic nematodes. Endogenous strategies to delay the negative effect of mating may represent a key evolutionary innovation to maximize reproductive success.

Data availability

Sequencing data have been deposited in NCBI SRA under accession code PRJNA508378

The following data sets were generated

Article and author information

Author details

  1. Lauren N Booth

    Department of Genetics, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  2. Travis J Maures

    Department of Genetics, Stanford University, Stanford, United States
    Competing interests
    Travis J Maures, is affiliated with Synthego. The author has no financial interests to declare..
  3. Robin W Yeo

    Department of Genetics, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  4. Cindy Tantilert

    Department of Genetics, Stanford University, Stanford, United States
    Competing interests
    No competing interests declared.
  5. Anne Brunet

    Department of Genetics, Stanford University, Stanford, United States
    For correspondence
    abrunet1@stanford.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4608-6845

Funding

National Institutes of Health (DP1 AG044848)

  • Anne Brunet

National Institutes of Health (R01 AG054201)

  • Anne Brunet

Helen Hay Whitney Foundation (Joan Whitney Payson Scholar)

  • Lauren N Booth

National Institutes of Health (K99 AG051738)

  • Lauren N Booth

Genentech Foundation (Genentech Foundation Predoctoral Fellow)

  • Robin W Yeo

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

Reviewing Editor

  1. Matt Kaeberlein, University of Washington, United States

Publication history

  1. Received: February 27, 2019
  2. Accepted: July 2, 2019
  3. Accepted Manuscript published: July 8, 2019 (version 1)
  4. Version of Record published: August 16, 2019 (version 2)

Copyright

© 2019, Booth 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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Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics
    George L Sutphin
    Insight

    Young Caenorhabditis elegans hermaphrodites use their own sperm to protect against the negative consequences of mating.

    1. Chromosomes and Gene Expression
    2. Evolutionary Biology
    Mathias Scharmann et al.
    Research Article Updated

    Differences between males and females are usually more subtle in dioecious plants than animals, but strong sexual dimorphism has evolved convergently in the South African Cape plant genus Leucadendron. Such sexual dimorphism in leaf size is expected largely to be due to differential gene expression between the sexes. We compared patterns of gene expression in leaves among 10 Leucadendron species across the genus. Surprisingly, we found no positive association between sexual dimorphism in morphology and the number or the percentage of sex-biased genes (SBGs). Sex bias in most SBGs evolved recently and was species specific. We compared rates of evolutionary change in expression for genes that were sex biased in one species but unbiased in others and found that SBGs evolved faster in expression than unbiased genes. This greater rate of expression evolution of SBGs, also documented in animals, might suggest the possible role of sexual selection in the evolution of gene expression. However, our comparative analysis clearly indicates that the more rapid rate of expression evolution of SBGs predated the origin of bias, and shifts towards bias were depleted in signatures of adaptation. Our results are thus more consistent with the view that sex bias is simply freer to evolve in genes less subject to constraints in expression level.