Neural Circuitry Underlying Drosophila Female Postmating Behavioral Responses

Carolina Rezával,Edward A Kravitz,Yick-Bun Chan,Stephen F Goodwin,Anthony J Dornan,Hania J Pavlou

doi:10.1016/j.cub.2012.04.062

Carolina Rezával, Edward A Kravitz + Show 4 more

Open Access

https://doi.org/10.1016/j.cub.2012.04.062

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Abstract

SummaryBackgroundAfter mating, Drosophila females undergo a remarkable phenotypic switch resulting in decreased sexual receptivity and increased egg laying. Transfer of male sex peptide (SP) during copulation mediates these postmating responses via sensory neurons that coexpress the sex-determination gene fruitless (fru) and the proprioceptive neuronal marker pickpocket (ppk) in the female reproductive system. Little is known about the neuronal pathways involved in relaying SP-sensory information to central circuits and how these inputs are processed to direct female-specific changes that occur in response to mating.ResultsWe demonstrate an essential role played by neurons expressing the sex-determination gene doublesex (dsx) in regulating the female postmating response. We uncovered shared circuitry between dsx and a subset of the previously described SP-responsive fru+/ppk+-expressing neurons in the reproductive system. In addition, we identified sexually dimorphic dsx circuitry within the abdominal ganglion (Abg) critical for mediating postmating responses. Some of these dsx neurons target posterior regions of the brain while others project onto the uterus.ConclusionsWe propose that dsx-specified circuitry is required to induce female postmating behavioral responses, from sensing SP to conveying this signal to higher-order circuits for processing and through to the generation of postmating behavioral and physiological outputs.

Highlights

In Drosophila, genes of the sex-determination hierarchy orchestrate the development and differentiation of sexspecific tissues, establishing sex-specific physiology and neural circuitry. doublesex and fruitless, two pivotal transcription factors of the sex determination hierarchy, establish most aspects of ‘‘maleness’’ and ‘‘femaleness’’ [1]
Our findings indicate that dsx circuitry consists of primary neurons required for sensing sex peptide (SP) in the reproductive system, and downstream effectors of the SP-sensory neuronal pathway that regulate postcopulatory behavior of females
These virgin females exhibited levels of receptivity comparable to mated control females (80% copulated within 1 hr) (Figure 1A)

Summary

Introduction

In Drosophila, genes of the sex-determination hierarchy orchestrate the development and differentiation of sexspecific tissues, establishing sex-specific physiology and neural circuitry. doublesex (dsx) and fruitless (fru), two pivotal transcription factors of the sex determination hierarchy, establish most aspects of ‘‘maleness’’ and ‘‘femaleness’’ [1]. In Drosophila, genes of the sex-determination hierarchy orchestrate the development and differentiation of sexspecific tissues, establishing sex-specific physiology and neural circuitry. Doublesex (dsx) and fruitless (fru), two pivotal transcription factors of the sex determination hierarchy, establish most aspects of ‘‘maleness’’ and ‘‘femaleness’’ [1]. While fru/dsx-expressing neurons have been shown to regulate male courtship behaviors [2,3,4,5], less is known about the circuitry underlying female mating. A receptive female will facilitate copulation by slowing down, ceasing rejection behaviors, and opening her vaginal plates [1]. While virgin females are highly receptive and rapidly copulate with a suitable partner, mated females undergo a substantial change in their physiology andbehavior, becoming temporarily sexually unreceptive to further copulatory attempts, while increasing oviposition [9]

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Discussion

Conclusion