Chemosensory adaptations in Caenorhabditis males during the establishment of androdioecy.

Abstract

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 Caenorhabditis species, we demonstrated that androdioecious hermaphrodites exhibit attenuated sex pheromone potency, while androdioecious males show heightened olfactory habituation and diminished mate exploration capabilities. The behaviour of androdioecious males can be reverted to resemble that of dioecious males by replacing the SRD-1 receptor with its dioecious orthologues. This intrinsic characteristic is contingent upon the C-terminal 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 confers a selective advantage favouring hermaphroditism. Our study provides insights into overlooked male traits, shaped by changes in chemosensory signalling. The findings underscore the capacity of chemosensory variations to influence how organisms perceive critical ecological factors, eventually facilitating the emergence and stabilization of hermaphroditism.