Regulation of Drosophila courtship behavior by the Tlx/tailless-like nuclear receptor, dissatisfaction

Julia C Duckhorn,Jessica Cande,Mary C Metkus,Hyeop Song,Sofia Altamirano,David L Stern,Troy R Shirangi

doi:10.1016/j.cub.2022.02.031

Abstract

Sexually dimorphic courtship behaviors in Drosophila melanogaster develop from the activity of the sexual differentiation genes, doublesex (dsx) and fruitless (fru), functioning with other regulatory factors that have received little attention. The dissatisfaction (dsf) gene encodes an orphan nuclear receptor homologous to vertebrate Tlx and Drosophila tailless that is critical for the development of several aspects of female- and male-specific sexual behaviors. Here, we report the pattern of dsf expression in the central nervous system and show that the activity of sexually dimorphic abdominal interneurons that co-express dsf and dsx is necessary and sufficient for vaginal plate opening in virgin females, ovipositor extrusion in mated females, and abdominal curling in males during courtship. We find that dsf activity results in different neuroanatomical outcomes in females and males, promoting and suppressing, respectively, female development and function of these neurons depending upon the sexual state of dsx expression. We posit that dsf and dsx interact to specify sex differences in the neural circuitry for dimorphic abdominal behaviors.

Highlights

The neural circuitry for sex-specific behaviors in Drosophila melanogaster is currently understood to be specified during development by transcriptional regulators encoded by the doublesex and fruitless genes.[1]
The dsf gene was first identified over 20 years ago, yet where and when dsf is precisely expressed in the Drosophila nervous system, which dsf-expressing neurons matter for courtship behavior, and how dsf contributes to the sexual differentiation of the nervous system are not known
We reexamined dsf mRNA expression in the adult CNS by in situ hybridization chain reaction (HCR), a robust, quantitative, and sensitive method to detect mRNAs in wholemounted tissues.[14–17]

Summary

Introduction

The neural circuitry for sex-specific behaviors in Drosophila melanogaster is currently understood to be specified during development by transcriptional regulators encoded by the doublesex (dsx) and fruitless (fru) genes.[1]. The male isoforms of dsx and fru direct the differentiation of neurons in the adult male CNS that are required for performance of male courtship behaviors.[2–6]. The female-specific isoform of the dsx gene together with the absence of male-specific fru build the neural pathways that direct female-specific sexual behaviors.[3,6–9]. The dissatisfaction (dsf) gene, for instance, which encodes an orphan nuclear receptor homologous to vertebrate Tlx and Drosophila tailless, is required for several aspects of femaleand male-specific reproductive behaviors.[12,13]. The dsf gene was first identified over 20 years ago, yet where and when dsf is precisely expressed in the Drosophila nervous system, which dsf-expressing neurons matter for courtship behavior, and how dsf contributes to the sexual differentiation of the nervous system are not known

Methods

Results

Discussion

Conclusion