Natural Variation in plep-1 Causes Male-Male Copulatory Behavior in C. Elegans

Luke M. Noble, Audrey S. Chang, Daniel McNelis, Max Kramer, Mimi Yen, Jasmine P. Nicodemus, David D. Riccardi, Patrick Ammerman, Matthew Phillips, Tangirul Islam, Matthew Rockman

Research output: Contribution to journalArticle

Abstract

In sexual species, gametes have to find and recognize one another. Signaling is thus central to sexual reproduction and involves a rapidly evolving interplay of shared and divergent interests [1-4]. Among Caenorhabditis nematodes, three species have evolved self-fertilization, changing the balance of intersexual relations [5]. Males in these androdioecious species are rare, and the evolutionary interests of hermaphrodites dominate. Signaling has shifted accordingly, with females losing behavioral responses to males [6, 7] and males losing competitive abilities [8, 9]. Males in these species also show variable same-sex and autocopulatory mating behaviors [6, 10]. These behaviors could have evolved by relaxed selection on male function, accumulation of sexually antagonistic alleles that benefit hermaphrodites and harm males [5, 11], or neither of these, because androdioecy also reduces the ability of populations to respond to selection [12-14]. We have identified the genetic cause of a male-male mating behavior exhibited by geographically dispersed C. Elegans isolates, wherein males mate with and deposit copulatory plugs on one another's excretory pores. We find a single locus of major effect that is explained by segregation of a loss-of-function mutation in an uncharacterized gene, plep-1, expressed in the excretory cell in both sexes. Males homozygous for the plep-1 mutation have excretory pores that are attractive or receptive to copulatory behavior of other males. Excretory pore plugs are injurious and hermaphrodite activity is compromised in plep-1 mutants, so the allele might be unconditionally deleterious, persisting in the population because the species' androdioecious mating system limits the reach of selection.

Original languageEnglish (US)
Pages (from-to)2730-2737
Number of pages8
JournalCurrent Biology
Volume25
Issue number20
DOIs
StatePublished - Oct 19 2015

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Deposits
Genes
Aptitude
mating behavior
germ cells
Caenorhabditis
Self-Fertilization
androdioecy
Alleles
alleles
Mutation
selfing
sexual reproduction
Germ Cells
mating systems
Population
Reproduction
Nematoda
mutation
mutants

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Noble, L. M., Chang, A. S., McNelis, D., Kramer, M., Yen, M., Nicodemus, J. P., ... Rockman, M. (2015). Natural Variation in plep-1 Causes Male-Male Copulatory Behavior in C. Elegans. Current Biology, 25(20), 2730-2737. https://doi.org/10.1016/j.cub.2015.09.019

Natural Variation in plep-1 Causes Male-Male Copulatory Behavior in C. Elegans. / Noble, Luke M.; Chang, Audrey S.; McNelis, Daniel; Kramer, Max; Yen, Mimi; Nicodemus, Jasmine P.; Riccardi, David D.; Ammerman, Patrick; Phillips, Matthew; Islam, Tangirul; Rockman, Matthew.

In: Current Biology, Vol. 25, No. 20, 19.10.2015, p. 2730-2737.

Research output: Contribution to journalArticle

Noble, LM, Chang, AS, McNelis, D, Kramer, M, Yen, M, Nicodemus, JP, Riccardi, DD, Ammerman, P, Phillips, M, Islam, T & Rockman, M 2015, 'Natural Variation in plep-1 Causes Male-Male Copulatory Behavior in C. Elegans', Current Biology, vol. 25, no. 20, pp. 2730-2737. https://doi.org/10.1016/j.cub.2015.09.019
Noble LM, Chang AS, McNelis D, Kramer M, Yen M, Nicodemus JP et al. Natural Variation in plep-1 Causes Male-Male Copulatory Behavior in C. Elegans. Current Biology. 2015 Oct 19;25(20):2730-2737. https://doi.org/10.1016/j.cub.2015.09.019
Noble, Luke M. ; Chang, Audrey S. ; McNelis, Daniel ; Kramer, Max ; Yen, Mimi ; Nicodemus, Jasmine P. ; Riccardi, David D. ; Ammerman, Patrick ; Phillips, Matthew ; Islam, Tangirul ; Rockman, Matthew. / Natural Variation in plep-1 Causes Male-Male Copulatory Behavior in C. Elegans. In: Current Biology. 2015 ; Vol. 25, No. 20. pp. 2730-2737.
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