Chemosensory Adaptations in Caenorhabditis Males during the Establishment of Androdioecy

Caenorhabditis elegans has evolved from its dioecious ancestors to adopt an androdioecious reproductive strategy. In this process, ancestral female C. elegans acquired genetic modifications that enabled self-sperm generation, self-sperm activation, and a reduced reliance on sexual reproduction. However, how males have adapted during this transition from dioecy to androdioecy is less explored. Using respective Caenorhabditis species, we demonstrated that androdioecious hermaphrodites exhibit a reduction in sex pheromone potency, while androdioecious males show notably heightened olfactory habituation and diminished mate exploration capabilities. The behavior of androdioecious males can be reverted to resemble that of dioecious males by replacing the SRD-1 receptor with its dioecious orthologs. This intrinsic characteristic is contingent upon the cytoplasmic domain of the receptor. We propose a theoretical framework where C. elegans males have accumulated genetic variations in their pheromone receptor, leading to altered chemosensory perception of the opposite sex, which confer a selective advantage that favors the establishment of hermaphroditism. Our study provides insights into an overlooked male trait that was shaped by changes in chemosensory signaling. The findings underscore the capacity of chemosensory variations to influence how organisms perceive critical ecological factors and eventually facilitate the emergence and stabilization of hermaphroditism.