Molecular Changes of a Chemosensory Component in Males that Facilitate the Mating System Transition from Dioecy to Androdioecy in Caenorhabditis Species

The nematode Caenorhabditis elegans has transitioned from a dioecious ancestry to an androdioecious reproductive system, wherein hermaphrodites possess the genetic capacity for self-sperm production, activation, and reduced dependence on mating. While the molecular adaptations enabling hermaphroditism are well characterized, the evolutionary trajectory of males during this shift remains less understood. Through comparative analyses across Caenorhabditis species, we reveal that androdioecious hermaphrodites display attenuated sex pheromone potency, whereas their male counterparts exhibit robust sex pheromone habituation and reduced mate-searching behaviour. Substitution of the SRD-1 receptor in androdioecious males with its dioecious orthologs restores ancestral dioecious male-like behaviour, implicating the receptor's C-terminal cytoplasmic domain in this functional divergence. We propose that C. elegans males have accumulated mutations in the sex pheromone specific receptor, altering their chemosensory perception of the opposite sex, which confers a selective advantage favouring hermaphroditism. These findings underscore the male-specific traits, that have been modulated by shifts in chemosensory signalling. These findings highlight how variations in sensory perception can reshape ecological interactions, ultimately contributing to the evolution and persistence of hermaphroditism.