Evolution remodels olfactory and mating-receptive behaviors in the transition from female to hermaphrodite reproduction.

Male/hermaphrodite species have arisen multiple times from a male/female ancestral state in nematodes, providing a model to study behavioral adaptations to different reproductive strategies. Here, we examined the mating behaviors of male/female (gonochoristic) Caenorhabditis species in comparison with male/hermaphrodite (androdiecious) close relatives. We find that females from two species in the Elegans group chemotax to volatile odor from males, but hermaphrodites do not. Females, but not hermaphrodites, also display known mating-receptive behaviors such as sedation when male reproductive structures contact the vulva. Focusing on the male/female species C. nigoni, we show that female chemotaxis to males is limited to adult females approaching adult or near-adult males and relies upon the AWA neuron-specific transcription factor ODR-7, as does male chemotaxis to female odor as previously shown in C. elegans. However, female receptivity during mating contact is odr-7 independent. All C. nigoni female behaviors are suppressed by mating and all are absent in young hermaphrodites from the sister species C. briggsae. However, latent receptivity during mating contact can be uncovered in mutant or aged C. briggsae hermaphrodites that lack self-sperm. These results reveal two mechanistically distinct components of the shift from female to hermaphrodite behavior: the loss of female-specific odr-7-dependent chemotaxis and a sperm-dependent state of reduced receptivity to mating contact. Hermaphrodites from a second androdioecious species, C. tropicalis, recover all female behaviors upon aging, including chemotaxis to males. Regaining mating receptivity after sperm depletion could maximize hermaphrodite fitness across their lifespan.