The complete synaptic-resolution connectome of the Drosophila male central nervous system reveals that sexual dimorphism is organized hierarchically, with sex-specific and dimorphic neurons concentrated in higher integrative brain centers rather than sensory-motor periphery, and that dimorphic connectivity propagates broadly through the brain involving 18% of male neurons despite only 5% being morphologically dimorphic, through tightly coupled network modules that create specialized circuit architectures for sex-specific behaviors across visual, auditory, olfactory, and gustatory modalities.

Sex differences in behaviour exist across all animals, typically under strong genetic regulation. In Drosophila, fruitless/doublesex transcription factors can identify dimorphic neurons but their organisation into functional circuits remains unclear.

We present the connectome of the entire Drosophila male central nervous system. This contains 166,691 neurons spanning the brain and nerve cord, fully proofread and annotated including fruitless/doublesex expression and 11,691 types. We provide the first comprehensive comparison between male and female brain connectomes to synaptic resolution, finding 7,205 isomorphic, 114 dimorphic, 262 male-specific and 69 female-specific types.

This resource enables analysis of full sensory-to-motor circuits underlying complex behaviours and the impact of dimorphic elements. Sex-specific/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 arbours. Numerous circuit switches reroute sensory information to form antagonistic circuits controlling opposing behaviours.