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

Abstract

Summary 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. As excretory pore plugs are injurious and hermaphrodite activity is compromised in plep-1 mutants, the allele may be unconditionally deleterious, persisting in the population because the species' androdioecious mating system limits the reach of selection.

Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins

“…Other changes in selfing species, such as loss of plg-1 and of plep-1, which mediates reliable male discrimination between the vulva and excretory pore (4, 6), are likely due to relaxed selection. However, restoring mss to C. briggsae enhances male fitness (Fig.…”

Tightly linked antagonistic-effect loci underlie polygenic phenotypic variation inC. elegans

“…; Noble et al. ; Zdraljevic et al. ), complex traits in C. elegans often have polygenic or otherwise complex architectures (Green et al.…”

“…These features allow for relatively quick construction of recombinant panels and high-throughput assays in 96-well plates . Although many traits in C. elegans have a simple genetic basis (e.g., Palopoli et al 2008;Ghosh et al 2012;Noble et al 2015;Zdraljevic et al 2017), complex traits in C. elegans often have polygenic or otherwise complex architectures (Green et al 2013;Glater et al 2014;Andersen et al 2015;Greene et al 2016;Evans et al 2018;Noble et al 2017).…”

The Caenorhabditis elegans Excretory System: A Model for Tubulogenesis, Cell Fate Specification, and Plasticity

“…The gland stains with the neurosecretory marker paraldehyde-fuschin (PAF) (Nelson et al 1983) and with the sterol-binding agents dehydroergosterol (DHE) and filipin (Merris et al 2003), consistent with steroid hormone production. In the absence of hermaphrodites, male plep-1 mutants attempt to copulate with the excretory pore of other males (Noble et al 2015), consistent with some attractive secretion emanating from the pore, and possibly originating in the gland. Singh and Sulston (1978) and Nelson and Riddle (1984) investigated the effects of gland ablation in larvae and found no disruption in osmoregulation, molting, dauer formation, or dauer exit, but other aspects of the animal's physiology or behavior were not examined.…”