A Sexually-dimorphic Brain Module for Sensory Integration

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The complex interplay between a male and female of a species during courtship is one of the most remarkable examples of sexually dimorphic behaviour in the animal kingdom. Upon identifying a suitable partner, Drosophila melanogaster males initiate an elaborate courtship ritual that culminates with copulation. Drosophila females do not actively court males, yet it is her response to the male's advances that determines whether mating will actually occur. These are complex decisions and behaviours controlled by the brain, but working with flies has the advantage of using a vast array of genetic tools that allows us to identify and manipulate relevant neurons in the brain. With these tools we can ask how does the brain differ between the sexes, and how might these differences explain the distinct behaviours of males and females that are critical for reproductive success? Sexually reproducing species exhibit sex differences in social interactions, ostensibly to boost reproductive success and survival of progeny. A core set of sex-typical behavioural displays such as mating, and aggression, although modifiable by experience, are innate in the sense that they can be displayed without prior training. How does an animal's biological sex instruct the behavioural response? Males and females transform sensory input into sexually dimorphic behaviours, suggesting that such behaviours are generated by neural circuits that differ between the sexes These sexual dimorphisms in innate behaviour reflect the action of a sexually differentiated nervous system. Animals determine sex early in their development, and sex determination initiates many irreversible sexual differentiation events that influence how the genome and the environment interact to give rise to sex-specific behaviours. Across taxa, such mechanisms converge to regulate sexually dimorphic gene expression that in turn specifies sex-typical development and neural circuit function.In the fly, sex-specific behaviours are hardwired into the nervous system via the actions of two sex determination transcription factors (TFs), Doublesex (Dsx) and Fruitless (Fru). We have focused our attention on neurons that express these TFs to find anatomical or molecular sex differences in neuronal populations in order to gain an entry point into the neural circuits underlying gender-typical behaviours and identify the neuronal nodes that control component behaviours and behavioural sequencing. Alternative neural circuit wiring configurations have been proposed to generate sexually dimorphic behaviours. Neurons present only in one sex (qualitative sex difference) may either activate or inhibit a sexually dimorphic behaviour in that sex. More commonly in invertebrates and vertebrates, a neuronal population is present in both sexes but presents sex differences (quantitative sex difference) in physiology, neuron number, or connectivity. In such cases, the neurons may regulate the probability of displaying a sexually dimorphic behaviour, or control the display of different sexually dimorphic behaviours in the two sexes (functionally bivalent). We have focused on the role of neurons that express dsx. These dsx+ neurons control male courtship behaviour and aspects of female receptivity. Yet little is known about the specific role of dsx+ neurons in the brain, which are believed to control mating decisions. We identified a group of sexually-dimorphic dsx neurons that are critical to sensory integration in males and females. Importantly, the dimorphism we uncovered can alter connectivity and information flow between males and females, where a dedicated visual pathway processing sex-specific visual cues has evolved in males, but not females.Our goal is to understand how neural circuits in general, and sexually dimorphic neurons in particular, can generate sexually dimorphic behaviours, and how molecular mechanisms and evolutionary constraints shape these behaviours.