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

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. •Wild isolates of C. elegans vary in a male-male mating behavior•In some isolates, males deposit copulatory plugs on each other’s excretory pores•A mutation in a conserved gene renders pores attractive or receptive to matings•Excretory pore plugging may be a side effect of mating system evolution Noble et al. identify the genetic cause of natural variation in male-male copulatory behavior in C. elegans. Males homozygous for a loss-of-function mutation in one member of a highly conserved gene family have excretory pores that are attractive or receptive to mating by other males. The gene, plep-1, is expressed in the excretory cell.