Males and females show significant differences in social behaviours, which depend on sex-specific neuronal organization. These differences are critical for reproduction, parenting and other basic interactions between animals. However, the neural circuitry underlying sexually dimorphic patterns is mostly unknown.
Sexually dimorphic behaviour in Drosophila is a key model system for revealing how genetically-determined properties of neuronal circuits define behaviour. Drosophila offers a unique model system to decipher the logic of dimorphic neuronal circuits, with its wealth of anatomical and neurogenetic tools, and a repertoire of dimorphic sexual behaviours. Although many sensory stimuli are integrated to regulate social behaviour, one of the best understood is the Drosophila male pheromone cVA, which promotes mating in females but repels other males and promotes inter-male aggression. Recent work from the host lab identified, for the first time, a sexually dimorphic switch in neuronal connectivity. The transcriptional master regulator fruitless rewires connections between pheromone responsive input neurons and two different target neuron populations in male and female brains. This study opened the question whether different target populations between males and females promote distinct behaviours. The current grant focused on three interdisciplinary aims that built on these results by establishing a causal role for specific wiring differences in regulating sexually dimorphic social behaviours; and studying how simple switches are assembled into more complex networks, at the interface of sensory processing and behavioural control.
The main research questions were how is the pheromone processing pathway organized in male and female brains, and how do differences in this pathway between male and female affect sexual behaviour. Understanding the logic of sexually dimorphic circuits also teaches us how simple circuit motifs are assembled into complex networks, from sensory input to behavioural output.
Conclusions of the action:
Using the emerging Drosophila connectome (Figure 1A), we reconstructed the neuroanatomical map of brain connections in the pheromone processing circuitry. This neuroanatomical wiring map spans from sensory neurons (olfactory, gustatory and mechanical) to descending neurons controlling motor output. Based on the wiring map we identified five novel sets of neurons in key points transmitting pheromone information. We then identified genetic driver lines for each of these subsets, tested the functionality of the connectivity using functional imaging, and manipulated these neuronal subsets in the brain while flies were freely behaving, in both sexes. We uncovered how each neuronal subset contributes to dimorphic social behaviours, including male-male aggression, male-female courtship, female receptivity, and female egg laying. Our work provides a direct link between anatomical differences and functional differences, and pinpoint the roles of specific circuit elements in regulating sexual behaviours.
