Abstract
Dioecious species are a hallmark of the animal kingdom, with opposing sexes responding differently to identical sensory cues. Here, we study the response of C. elegans to the small-molecule pheromone, ascr#8, which elicits opposing behavioral valences in each sex. We identify a novel neuropeptide-neuropeptide receptor (NP/NPR) module that is active in males, but not in hermaphrodites. Using a novel paradigm of neuropeptide rescue that we established, we leverage bacterial expression of individual peptides to rescue the sex-specific response to ascr#8. Concurrent biochemical studies confirmed individual FLP-3 peptides differentially activate two divergent receptors, NPR-10 and FRPR-16. Interestingly, the two of the peptides that rescued behavior in our feeding paradigm are related through a conserved threonine, suggesting that a specific NP/NPR combination sets a male state, driving the correct behavioral valence of the ascr#8 response. Receptor expression within pre-motor neurons reveals novel coordination of male-specific and core locomotory circuitries.
Highlights
Dioecious species are a hallmark of the animal kingdom, with opposing sexes responding differently to identical sensory cues
We first compared the attractiveness of 1 μM ascr#8 (Fig. 1a, inset) across multiple strains of C. elegans, using our novel behavioral assay, the single worm attraction assay (SWAA) (Fig. 1a)
Our results reveal a complex mechanism regulating the sexspecific behavioral response to a pheromone guided through the interaction of at least two peptides encoded by a singleneuropeptide precursor gene and two divergent GPCRs
Summary
Dioecious species are a hallmark of the animal kingdom, with opposing sexes responding differently to identical sensory cues. The vomeronasal and main olfactory epithelium in mice are required for male aggression and mating, but in females they contribute towards receptivity and aggression[3] Prominent among these stimuli are mating cues[4]; while the visual displays of higher order animals are among the most apparent of these, chemical mating cues are the most ubiquitous, with entire sensory organs dedicated to pheromone sensation[5]. Nematodes communicate through a large and growing class of pheromones termed ascarosides (ascr)[6] These small molecules convey social as well as developmental information, and the assays used to understand the roles of these cues have varied[4,6]
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