Abstract

BackgroundMating behaviors in simple invertebrate model organisms represent tractable paradigms for understanding the neural bases of sex-specific behaviors, decision-making and sensorimotor integration. However, there are few examples where such neural circuits have been defined at high resolution or interrogated.Methodology/Principal FindingsHere we exploit the simplicity of the nematode Caenorhabditis elegans to define the neural circuits underlying the male’s decision to initiate mating in response to contact with a mate. Mate contact is sensed by male-specific sensilla of the tail, the rays, which subsequently induce and guide a contact-based search of the hermaphrodite’s surface for the vulva (the vulva search). Atypically, search locomotion has a backward directional bias so its implementation requires overcoming an intrinsic bias for forward movement, set by activity of the sex-shared locomotory system. Using optogenetics, cell-specific ablation- and mutant behavioral analyses, we show that the male makes this shift by manipulating the activity of command cells within this sex-shared locomotory system. The rays control the command interneurons through the male-specific, decision-making interneuron PVY and its auxiliary cell PVX. Unlike many sex-shared pathways, PVY/PVX regulate the command cells via cholinergic, rather than glutamatergic transmission, a feature that likely contributes to response specificity and coordinates directional movement with other cholinergic-dependent motor behaviors of the mating sequence. PVY/PVX preferentially activate the backward, and not forward, command cells because of a bias in synaptic inputs and the distribution of key cholinergic receptors (encoded by the genes acr-18, acr-16 and unc-29) in favor of the backward command cells.Conclusion/SignificanceOur interrogation of male neural circuits reveals that a sex-specific response to the opposite sex is conferred by a male-specific pathway that renders subordinate, sex-shared motor programs responsive to mate cues. Circuit modifications of these types may make prominent contributions to natural variations in behavior that ultimately bring about speciation.

Highlights

  • Courtship and mating are among the most elaborate of behaviors displayed in the animal kingdom [1]

  • Sensory control of directional movement in C. elegans provides a tractable system for exploring this issue and has been the subject of intense investigation in the hermaphrodite

  • We examine this issue in the context of a sex-specific behavior and ask: how do mate contact cues override the forward locomotion bias of exploratory behavior and induce the male to pursue sex? Mate contact, sensed by the rays, causes the male to abruptly switch from forward to backward movement in order to conduct a systematic, contact-based search for the vulva

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Summary

Introduction

Courtship and mating are among the most elaborate of behaviors displayed in the animal kingdom [1]. The ultimate goal of the male in these behaviors is to fertilize oocytes Achieving this goal often requires the execution of a behavioral sequence, progression through which depends on detection of appropriate conspecific cues and the expression of appropriate behavioral responses [2]. These sequences serve to ensure that copulation occurs between conspecifics and that unworthy or inappropriate partners are rejected. The study of mating behavior can provide valuable insight into understanding the neural bases of sex-specific behaviors, and mechanisms underlying decision-making, sensorimotor integration and the coordinated timing of sequenced motor behaviors. Mating behaviors in simple invertebrate model organisms represent tractable paradigms for understanding the neural bases of sex-specific behaviors, decision-making and sensorimotor integration. There are few examples where such neural circuits have been defined at high resolution or interrogated

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