Background Adaptive behavioral prioritization requires flexible outputs from fixed neural circuits. In C. elegans, the prioritization of feeding vs. mate-searching depends on biological sex (males will abandon food to search for mates, while hermaphrodites will not) as well as developmental stage and feeding status. Previously, we found that males are less attracted than hermaphrodites to the food-associated odorant diacetyl, suggesting that sensory modulation may contribute to behavioral prioritization. Results We find that somatic sex acts cell-autonomously to reconfigure the olfactory circuit by regulating a key chemoreceptor, odr-10, in the AWA neurons. Moreover, we find that odr-10 has a significant role in food detection, the regulation of which contributes to sex differences in behavioral prioritization. Overexpression of odr-10 increases male food attraction and decreases off-food exploration; conversely, odr-10 loss impairs food taxis in both sexes. In larvae, both sexes prioritize feeding over exploration; correspondingly, the sexes have equal odr-10 expression and food attraction. Food deprivation, which transiently favors feeding over exploration in adult males, increases male food attraction by activating odr-10 expression. Furthermore, the weak expression of odr-10 in well-fed adult males has important adaptive value, allowing males to efficiently locate mates in a patchy food environment. Conclusions We find that modulated expression of a single chemoreceptor plays a key role in naturally occurring variation in the prioritization of feeding and exploration. The convergence of three independent regulatory inputs—somatic sex, age, and feeding status—on chemoreceptor expression highlights sensory function as a key source of plasticity in neural circuits.

No abstract

Although sexual dimorphism is ubiquitous in animals, the means by which sex determination mechanisms trigger specific modifications to shared structures is not well understood. In C. elegans, tail tip morphology is highly dimorphic: whereas hermaphrodites have a whip-like, tapered tail tip, the male tail is blunt-ended and round. Here we show that the male-specific cell fusion and retraction that generate the adult tail are controlled by the previously undescribed doublesex-related DM gene dmd-3, with a secondary contribution from the paralogous gene mab-3. In dmd-3 mutants, cell fusion and retraction in the male tail tip are severely defective, while in mab-3; dmd-3 double mutants, these processes are completely absent. Conversely, expression of dmd-3 in the hermaphrodite tail tip is sufficient to trigger fusion and retraction. The master sexual regulator tra-1 normally represses dmd-3 expression in the hermaphrodite tail tip, accounting for the sexual specificity of tail tip morphogenesis. Temporal cues control the timing of tail remodeling in males by regulating dmd-3 expression, and Wnt signaling promotes this process by maintaining and enhancing dmd-3 expression in the tail tip. Downstream, dmd-3 and mab-3 regulate effectors of morphogenesis including the cell fusion gene eff-1. Together, our results reveal a regulatory network for male tail morphogenesis in which dmd-3 and mab-3 together occupy the central node. These findings indicate that an important conserved function of DM genes is to link the general sex determination hierarchy to specific effectors of differentiation and morphogenesis.