Activation of Latent Courtship Circuitry in the Brain of Drosophila Females Induces Male-like Behaviors

Carolina Rezával,Siddharth Pattnaik,Hania J Pavlou,Tetsuya Nojima,Birgit Brüggemeier,Luis A.D D’Souza,Hany K.M Dweck,Stephen F Goodwin

doi:10.1016/j.cub.2016.07.021

Carolina Rezával, Siddharth Pattnaik + Show 6 more

Open Access

https://doi.org/10.1016/j.cub.2016.07.021

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Abstract

SummaryCourtship in Drosophila melanogaster offers a powerful experimental paradigm for the study of innate sexually dimorphic behaviors [1, 2]. Fruit fly males exhibit an elaborate courtship display toward a potential mate [1, 2]. Females never actively court males, but their response to the male’s display determines whether mating will actually occur. Sex-specific behaviors are hardwired into the nervous system via the actions of the sex determination genes doublesex (dsx) and fruitless (fru) [1]. Activation of male-specific dsx/fru+ P1 neurons in the brain initiates the male’s courtship display [3, 4], suggesting that neurons unique to males trigger this sex-specific behavior. In females, dsx+ neurons play a pivotal role in sexual receptivity and post-mating behaviors [1, 2, 5, 6, 7, 8, 9]. Yet it is still unclear how dsx+ neurons and dimorphisms in these circuits give rise to the different behaviors displayed by males and females. Here, we manipulated the function of dsx+ neurons in the female brain to investigate higher-order neurons that drive female behaviors. Surprisingly, we found that activation of female dsx+ neurons in the brain induces females to behave like males by promoting male-typical courtship behaviors. Activated females display courtship toward conspecific males or females, as well other Drosophila species. We uncovered specific dsx+ neurons critical for driving male courtship and identified pheromones that trigger such behaviors in activated females. While male courtship behavior was thought to arise from male-specific central neurons, our study shows that the female brain is equipped with latent courtship circuitry capable of inducing this male-specific behavioral program.

Highlights

We assessed the behavioral effects of activating brain dsx+ neurons by expressing the heat-activated ion channel TrpA1, which induces depolarization when the temperature is increased above 25C [14]
While wild-type D. melanogaster females never display male courtship behaviors, we found that dsxbrain>TrpA1 females spend $50% of their time courting males, performing the first steps of the behavioral ritual, such as following and tapping the target fly, as well as extending one or two wings (Figure S1)
Most males targeted by the activated females showed greatly reduced levels of courtship and instead attempted to escape the female’s advances (Figures 1E and S1; Movie S2). dsxbrain>TrpA1 females were attracted to wild-type females (Movie S3), showing no sexspecific bias in their behavioral response, as they spent a similar amount of time courting each sex in a preference assay (Figure 1F)

Summary

Introduction

When thermally activated (at 33C), dsxbrain>TrpA1 virgin females showed male-typical behaviors toward males (Figures 1E and S1; Movie S2). While wild-type D. melanogaster females never display male courtship behaviors, we found that dsxbrain>TrpA1 females spend $50% of their time courting males, performing the first steps of the behavioral ritual, such as following and tapping the target fly, as well as extending one or two wings (Figure S1). Dsxbrain>TrpA1 females were attracted to wild-type females (Movie S3), showing no sexspecific bias in their behavioral response, as they spent a similar amount of time courting each sex in a preference assay (Figure 1F).

Results

Conclusion