Sexually dimorphic neuromodulation is emerging as a key determinant of sex differences in behavior. However, little is known about the mechanisms by which genetic sex tunes the functional properties of shared circuitry. To approach this issue, we are studying sexually dimorphic responses to ascaroside sex pheromones in C. elegans. Previous work has shown that a mixture of ascarosides ascr#2, #3 and #8 elicits strong attraction in males but weakly repels hermaphrodites. By studying sexually mosaic animals, we have discovered that the circuitry eliciting this attraction is present in both sexes but is functionally silent in hermaphrodites. That is, switching the sexual state of shared circuits is sufficient to switch the sexual phenotype of ascaroside attraction behavior. Moreover, we have found that sexual state is particularly important in the sensory neuron ADF, previously implicated in dauer entry. Feminizing ADF alone causes a complete loss of male attraction, while masculinizing it is sufficient to generate attraction in hermaphrodites. Consistent with this, ablation of ADF in males eliminates attraction. However, the serotonergic function of ADF does not appear to be required for pheromone attraction. Through a candidate screen to identify factors important for ADF’s sexually dimorphic function, we found that signaling by the neuropeptides PDF-1 and PDF-2 promotes ascaroside attraction. Interestingly, this pathway appears to act through distinct mechanisms to promote male attraction and to repress hermaphrodite repulsion. The mammalian ortholog of the these neuropeptides, VIP, is enriched in the male hypothalamus, suggesting this may reflect a conserved sex-dependent neuromodulatory mechanism.
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