Mating and Male pheromone kill Caenorhabditis males through distinct mechanisms

  1. Cheng Shi
  2. Alexi M Runnels
  3. Coleen T Murphy  Is a corresponding author
  1. Princeton University, United States

Abstract

Differences in longevity between sexes is a mysterious yet general phenomenon across great evolutionary distances. To test the roles of responses to environmental cues and sexual behaviors in longevity regulation, we examined Caenorhabditis male lifespan under solitary, grouped, and mated conditions. We find that neurons and the germline are required for male pheromone-dependent male death. Hermaphrodites with a masculinized nervous system secrete male pheromone and are susceptible to male pheromone killing. Male pheromone-mediated killing is unique to androdioecious Caenorhabditis, and may reduce the number of males in hermaphroditic populations; neither males nor females of gonochoristic species are susceptible to male pheromone killing. By contrast, mating-induced death, which is characterized by germline-dependent shrinking, glycogen loss, and ectopic vitellogenin expression, utilizes distinct molecular pathways and is shared between the sexes and across species. The study of sex- and species-specific regulation of aging reveals deeply conserved mechanisms of longevity and population structure regulation.

Article and author information

Author details

  1. Cheng Shi

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0365-8273
  2. Alexi M Runnels

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8592-1444
  3. Coleen T Murphy

    Department of Molecular Biology, Princeton University, Princeton, United States
    For correspondence
    ctmurphy@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8257-984X

Funding

Glenn Foundation for Medical Research (NA)

  • Cheng Shi
  • Coleen T Murphy

National Institutes of Health (DP1 GM119167-02)

  • Cheng Shi
  • Alexi M Runnels
  • Coleen T Murphy

Howard Hughes Medical Institute (Faculty Scholars Award)

  • Coleen T Murphy

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

Reviewing Editor

  1. Andrew Dillin, Howard Hughes Medical Institute, University of California, Berkeley, United States

Version history

  1. Received: November 19, 2016
  2. Accepted: March 4, 2017
  3. Accepted Manuscript published: March 14, 2017 (version 1)
  4. Accepted Manuscript updated: March 16, 2017 (version 2)
  5. Version of Record published: April 3, 2017 (version 3)

Copyright

© 2017, Shi 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

  • 3,733
    views
  • 654
    downloads
  • 49
    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. Cheng Shi
  2. Alexi M Runnels
  3. Coleen T Murphy
(2017)
Mating and Male pheromone kill Caenorhabditis males through distinct mechanisms
eLife 6:e23493.
https://doi.org/10.7554/eLife.23493

Share this article

https://doi.org/10.7554/eLife.23493