Dynamic Regulation of Adult-Specific Functions of the Nervous System by Signaling from the Reproductive System

Unlike juveniles, adult animals engage in suites of behaviors related to the search for and selection of potential mates and mating, including appropriate responses to sex pheromones. As in other species [1], male sex pheromones modulate several behaviors and physiological processes in C. elegans hermaphrodites [2–5]. In particular, one of these small-molecule signals, an ascaroside ascr#10, causes reduced exploration, more avid mating, and improved reproductive performance (see the accompanying paper by Aprison and Ruvinsky in this issue of Current Biology) [6]. Here, we investigated the mechanism that restricts pheromone response to adult hermaphrodites. Unexpectedly, we found that attainment of developmental adulthood was not alone sufficient for the behavioral response to the pheromone. To modify exploratory behavior in response to male pheromone, adult hermaphrodites also require functional germline and egg-laying apparatus. We show that this dependence of behavior on the reproductive system is due to feedback from the vulva muscles that reports ongoing reproduction to the nervous system. Our results reveal an activity-dependent conduit by which the reproductive system continuously licenses adult behaviors, including appropriate responses to the pheromones of the opposite sex. More broadly, our results suggest that signals from peripheral organs may serve as an important component of assuring age-appropriate functions of the nervous system.