Fertility reversibly modulates C. elegans behavior via gonad-nervous system signaling

While the external cues that generate behavioral responses have been extensively studied, behavioral changes in response to internal stimuli are much less understood. C. elegans hermaphrodites are self-fertile until they exhaust their supply of self-sperm, after which time they can only produce more progeny via mating with a male animal. Fertile hermaphrodites are less likely to be mated by males than sperm-exhausted hermaphrodites. We report that sperm-dependent hermaphrodite escape is facilitated by an aversive response to physical contact (touch stimulus) by males, specifically male turns around the hermaphrodite nose and male contact at the vulva. Using germline masculinizing and feminizing mutants, we found that sperm are both necessary and sufficient to induce contact-dependent mating evasion. Surprisingly, loss of the entire somatic gonad resulted in ectopic evasion behavior, via an oppositional monoaminergic signal. Hermaphrodites lacking the HSN neuron are constitutively receptive to male mating touch both at the vulva and at the nose, suggesting that HSN transmits fertility status to the nervous system. HSN also modulates other downstream circuits, such as the nose touch sensory neurons ASH and FLP, which are required for evasion of male contact at the nose. Taken together, we identified a signaling cascade wherein presence vs. absence of sperm is transmitted via monoaminergic signaling from the somatic gonad to the nervous system. This demonstrates how changes in internal state, such as fertility status, act to modulate neural circuits and alter the valence of sensory input.