Evolutionary transitions from female to hermaphrodite reproduction remodel olfactory and mating-receptive behaviors

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 to male/hermaphrodite (androdiecious) close relatives. We find that females from two species in the Elegans group chemotax to volatile odor from males, a behavior described in only a few animal species. The females 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 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. Young hermaphrodites from a second androdioecious species, C. tropicalis, are similarly unreceptive to males, but recover all female behaviors upon aging. 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. The recovery of receptivity after sperm depletion has the potential to maximize hermaphrodite fitness across the lifespan. HighlightsO_LIFemale and hermaphrodite mating behaviors differ in closely related nematode species C_LIO_LIFemales are attracted to volatile male odors, but hermaphrodites are not C_LIO_LIThe same olfactory neuron pair drives female attraction to males and vice versa C_LIO_LILatent female mating behaviors are revealed in hermaphrodites that lack self-sperm C_LI