Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. From a male's perspective, sexual selection can optimize reproductive success by acting on the variance in mating success (pre-insemination selection) as well as the variance in fertilization success (post-insemination selection). The balance between pre- and post-insemination selection has not yet been investigated using a strong hypothesis-testing framework that directly quantifies the effects of post-insemination selection on the evolution of reproductive success. Here we use experimental evolution of a uniquely engineered genetic system that allows sperm production to be turned off and on in obligate male-female populations of Caenorhabditis elegans. We show that enhanced post-insemination competition increases the efficacy of selection and surpasses pre-insemination sexual selection in driving a polygenic response in male reproductive success. We find that after 30 generations post-insemination selection increased male reproductive success by an average of 5- to 7-fold. Contrary to expectation, enhanced pre-insemination competition hindered selection and slowed the rate of evolution. Furthermore, we found that post-insemination selection resulted in a strong polygenic response at the whole-genome level. Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness. Therefore, explicit consideration should be given to post-insemination dynamics when considering the population effects of sexual selection.

Mating is vital for sexually reproducing species, yet the ideal mating strategy for males and females can differ. The ensuing conflict between the sexes – namely, sexual conflict – results in a decrease in population level fitness. The degree of sexual conflict can be affected by the behavior, physiology, and life history of a population. Previous studies in the nematode Caenorhabditis elegans have shown that mating causes lifespan to decrease in pseudo-females and hermaphrodites, which was interpreted as evidence of sexual conflict. However, it is still an open question whether variations in mating condition and strain type can affect the degree of sexual conflict and lifespan decrease. Here, I investigate whether lifespan is affected by mating in conditions other than sex- skewed individual mating scenarios used in previous work. I conducted population-based mating assays in two different strains of C. elegans using both natural and male-skewed sex ratios. Counter to expectations, I found no effect of mating on lifespan in a wild isolate of C. elegans, while virgins from a canonical laboratory strain had a decreased lifespan relative to their counterparts mated in groups. My data offers a counterpoint to the literature, which agrees that mating universally decreases the lifespan of C. elegans pseudo-females and hermaphrodites. These results highlight the flexibility of reproductive costs and the importance of life histories in experimental populations.

Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. From a male’s perspective, sexual selection can optimize reproductive success by acting on the variance in mating success (pre-insemination selection) as well as the variance in fertilization success (post-insemination selection). The balance between pre- and post-insemination selection has not yet been investigated using a strong hypothesis-testing framework that directly quantifies the effects of post-insemination selection on the evolution of reproductive success. Here we use experimental evolution of a uniquely engineered genetic system that allows sperm production to be turned off and on in obligate male-female populations of Caenorhabditis elegans. We show that enhanced post-insemination competition increases the efficacy of selection and surpasses pre-insemination sexual selection in driving a polygenic response in male reproductive success. We find that after 10 selective events occurring over 30 generations post-insemination selection increased male reproductive success by an average of 5- to 7-fold. Contrary to expectation, enhanced pre-insemination competition hindered selection and slowed the rate of evolution. Furthermore, we found that post-insemination selection resulted in a strong polygenic response at the whole-genome level. Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness. Therefore, explicit consideration should be given to post-insemination dynamics when considering the population effects of sexual selection.