The Sensory Circuitry for Sexual Attraction in C. elegans Males

BACKGROUND Why do males and females behave differently? Sexually dimorphic behaviors could arise from sex-specific neurons or by the modification of circuits present in both sexes. C. elegans males exhibit different behaviors than hermaphrodites. Although there is a single class of sex-specific sensory neurons in the head of males, most of their neurons are part of a core nervous system also present in hermaphrodites. Are the behavioral differences due to sex-specific or core neurons? RESULTS We demonstrate that C. elegans males chemotax to a source of hermaphrodite pheromones. This sexual-attraction behavior depends on a TRPV (transient receptor potential vanilloid) channel encoded by the osm-9, ocr-1, and ocr-2 genes. OSM-9 is required in three classes of sensory neurons: the AWA and AWC olfactory neurons and the male-specific CEM neurons. The absence of OSM-9 from any of these neurons impairs attraction, suggesting that their ensemble output elicits sexual attraction. Likewise, the ablation of any of these classes after sexual maturation impairs attraction behavior. If ablations are performed before sexual maturation, attraction is unimpaired, demonstrating that these neurons compensate for one another. Thus, males lacking sex-specific neurons are still attracted to pheromones, suggesting that core neurons are sexualized. Similarly, transgender nematodes-animals that appear morphologically to be hermaphrodites but have a masculinized core nervous system-are attracted to hermaphrodite pheromones. CONCLUSIONS Both sexually dimorphic and core sensory neurons are normally required in the adult for sexual attraction, but they can replace each other during sexual maturation if necessary to generate robust male-specific sexual attraction behavior.