A Male Expressed Copulatory Plug Increases Female Fertility in Caenorhabditis Nematodes

The genomes of self-fertilizing hermaphrodites offer a unique opportunity to probe why some genes with sex-specific functions are lost while others are maintained. In the androdiecious species, Caenorhabditis elegans, the presence of mate plugging is polymorphic across genetic backgrounds. The production of a mating plug is controlled by a single gene, plg-1, which has male-specific expression. Given that males are present less than 1% of the time, this gene is likely lost through relaxed selection or purifying selection, especially if mate plugging is maintained through intrasexual selection in males as is often hypothesized. We capitalized on a diverse panel of almost 2,000 C. elegans natural strains to show that plg-1 is maintained in at least 61% of genetic backgrounds, despite the androdiecious mating system. Genetic diversity estimates suggest that the loss of plg-1 is correlated with species globalization. We show that hermaphrodite total fecundity is not correlated with plg-1 genotype, indicating that this gene is not being maintained through linkage to a hermaphrodite beneficial gene. We then demonstrate in both C. elegans and the obligate outcrossing species, C. remanei, that the presence of a mating plug does not assure paternity by preventing subsequent males from mating. Instead, females with a mating plug have an extended peak reproductive window and higher fecundity than females without a mating plug. Together, these results indicate that mate plugging is female beneficial. We suggest that this benefit is derived from mating plugs acting as a vulval cover that can inhibit sperm loss during egg laying, thus reducing sperm limitation. Our work indicates that mate plugging may not always invoke male competition and can instead represent reproductive cooperation. More broadly, it demonstrates that male-specific gene expression does not equate to male-specific function, especially in the context of reproductive interactions.