Coordinated Behavioral and Physiological Responses to a Social Signal Are Regulated by a Shared Neuronal Circuit

Successful reproduction in animals requires orchestration of behavior and physiological processes. Pheromones can induce both "releaser" (behavioral) and "priming" (physiological) effects [1] in vertebrates [2, 3] and invertebrates [4, 5]. Therefore, understanding the mechanisms underlying pheromone responses could reveal how reproduction-related behaviors and physiology are coordinated. Here, we describe a neuronal circuit that couples the reproductive system and behavior in adult Caenorhabditis elegans hermaphrodites. We found that the response of the oogenic germline to the male pheromone requires serotonin signal from NSM and HSN neurons that acts via the mod-1 receptor in AIY and RIF interneurons and is antagonized by pigment-dispersing factor (PDF). Surprisingly, the same neurons and pathways have been previously implicated in regulation of exploratory behavior in the absence of male-produced signals [6]. We demonstrate that male pheromone acts via this circuit in hermaphrodites to reduce exploration and decrease mating latency, thereby tuning multiple fitness-proximal processes. Our results demonstrate how a single circuit could coordinate behavioral and physiological responses to the environment, even those that unfold on different timescales. Our findings suggest the existence of a centralized regulatory mechanism that balances organismal resources between reproductive investment and somatic maintenance.