Mating strategies in Caenorhabditis elegans populations are determined by male developmental history

Mating strategies, whether sexual or asexual, confer unique costs and benefits to populations and species that facilitate evolutionary processes. In wild isolates of Caenorhabditis elegans, mating strategies are dependent on developmental history. Outcrossing significantly increases when one or both parents have transiently passed through the stress-resistant dauer diapause stage. However, the mechanisms of how life history alters mating strategies have not been systematically explored. Sex-specific responses to pheromones are a major driver of mating behaviors in C. elegans. We demonstrated previously that postdauer hermaphrodites exhibit a decreased avoidance of the pheromone ascr#3 due to the downregulation of the osm-9 TRPV channel gene in postdauer ADL neurons. Thus, we hypothesized that altered responses to pheromones in postdauer animals contribute to increased outcrossing. We conducted mating assays using wild type N2 Bristol, as well as osm-9, daf-3/co-SMAD, and mut-16/Mutator mutant strains that regulate the activity of hermaphrodite ADL neurons. First, we show that the outcrossing level of N2 Bristol correlated with the developmental history of males, and that postdauer males exhibited an increased ability to detect mates via pheromones compared to control males. In addition, DAF-3 plays a critical role in postdauer males to regulate mating, while playing a more minor role in hermaphrodites. Furthermore, mut-16 adults exhibited decreased outcrossing, and attempts to rescue the outcrossing phenotype resulted in transgenerational sterility due to defects in hermaphrodite and male germlines. Together, our results suggest a model whereby mating strategy is driven by male developmental history under combinatorial control of TGF-β and RNAi pathways.