1. Evolutionary Biology
  2. Genetics and Genomics

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
https://doi.org/10.7554/eLife.46418
Share this article
Cite this article
  1. Lauren N Booth
  2. Travis J Maures
  3. Robin W Yeo
  4. Cindy Tantilert
  5. Anne Brunet
(2019)
Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
eLife 8:e46418.
https://doi.org/10.7554/eLife.46418
  2. Download BibTeX
  3. Download .RIS

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

Version 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.

Metrics

  • 2,825
    views
  • 375
    downloads
  • 20
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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)

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

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

  1. Lauren N Booth
  2. Travis J Maures
  3. Robin W Yeo
  4. Cindy Tantilert
  5. Anne Brunet
(2019)
Self-sperm induce resistance to the detrimental effects of sexual encounters with males in hermaphroditic nematodes
eLife 8:e46418.
https://doi.org/10.7554/eLife.46418

Share this article

https://doi.org/10.7554/eLife.46418

Categories and tags

Research organism

Further reading

    1. Genetics and Genomics

    Insulin-like peptides and the mTOR-TFEB pathway protect Caenorhabditis elegans hermaphrodites from mating-induced death

    Cheng Shi, Lauren N Booth, Coleen T Murphy
    Research Article Updated

    Lifespan is shortened by mating, but these deleterious effects must be delayed long enough for successful reproduction. Susceptibility to brief mating-induced death is caused by the loss of protection upon self-sperm depletion. Self-sperm maintains the expression of a DAF-2 insulin-like antagonist, INS-37, which promotes the nuclear localization of intestinal HLH-30/TFEB, a key pro-longevity regulator. Mating induces the agonist INS-8, promoting HLH-30 nuclear exit and subsequent death. In opposition to the protective role of HLH-30 and DAF-16/FOXO, TOR/LET-363 and the IIS-regulated Zn-finger transcription factor PQM-1 promote seminal-fluid-induced killing. Self-sperm maintenance of nuclear HLH-30/TFEB allows hermaphrodites to resist mating-induced death until self-sperm are exhausted, increasing the chances that mothers will survive through reproduction. Mothers combat males’ hijacking of their IIS pathway by expressing an insulin antagonist that keeps her healthy through the activity of pro-longevity factors, as long as she has her own sperm to utilize.

    1. Evolutionary Biology
    2. Genetics and Genomics

    Aging: A new defense in the battle of the sexes

    George L Sutphin
    Insight

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

    1. Developmental Biology
    2. Evolutionary Biology

    The rapidly evolving X-linked MIR-506 family fine-tunes spermatogenesis to enhance sperm competition

    Zhuqing Wang, Yue Wang ... Wei Yan
    Research Article

    Despite rapid evolution across eutherian mammals, the X-linked MIR-506 family miRNAs are located in a region flanked by two highly conserved protein-coding genes (SLITRK2 and FMR1) on the X chromosome. Intriguingly, these miRNAs are predominantly expressed in the testis, suggesting a potential role in spermatogenesis and male fertility. Here, we report that the X-linked MIR-506 family miRNAs were derived from the MER91C DNA transposons. Selective inactivation of individual miRNAs or clusters caused no discernible defects, but simultaneous ablation of five clusters containing 19 members of the MIR-506 family led to reduced male fertility in mice. Despite normal sperm counts, motility, and morphology, the KO sperm were less competitive than wild-type sperm when subjected to a polyandrous mating scheme. Transcriptomic and bioinformatic analyses revealed that these X-linked MIR-506 family miRNAs, in addition to targeting a set of conserved genes, have more targets that are critical for spermatogenesis and embryonic development during evolution. Our data suggest that the MIR-506 family miRNAs function to enhance sperm competitiveness and reproductive fitness of the male by finetuning gene expression during spermatogenesis.