Sexual dimorphism in the complete connectome of the Drosophila male central nervous system

Sex differences in behaviour exist across the animal kingdom, typically under strong genetic regulation. In Drosophila , previous work has shown that fruitless and doublesex transcription factors identify neurons driving sexually dimorphic behaviour. However, the organisation of dimorphic neurons into functional circuits remains unclear. We now present the connectome of the entire Drosophila male central nervous system. This contains 166,696 neurons spanning the brain and ventral nerve cord, fully proofread and comprehensively annotated including fruitless and doublesex expression and 11,691 cell types. By comparison with a previous female brain connectome, we provide the first comprehensive description of the differences between male and female brains to synaptic resolution. Of 7,319 cross-matched cell types in the central brain, 114 are dimorphic with an additional 262 male- and 69 female-specific (totalling 3.8% of neurons in males and 1.9% in females). This resource enables analysis of full sensory-to-motor circuits underlying complex behaviours as well as the impact of dimorphic elements. Sex-specific and dimorphic neurons are concentrated in higher brain centres while the sensory and motor periphery are largely isomorphic. Within higher centres, male-specific connections are organised into hotspots defined by male-specific neurons or the presence of male-specific arbours on neurons that are otherwise similar between sexes. Numerous circuit switches reroute sensory information to form conserved, antagonistic circuits controlling opposing behaviours.