Developmental remodeling repurposes larval neurons for sexual behaviors in adult Drosophila

Most larval neurons in Drosophila are repurposed during metamorphosis for functions in adult life, but their contribution to the neural circuits for sexually dimorphic behaviors is unknown. Here, we identify two interneurons in the nerve cord of adult Drosophila females that control ovipositor extrusion, a courtship rejection behavior performed by mated females. We show that these two neurons are present in the nerve cord of larvae as mature, sexually monomorphic interneurons. During pupal development, they acquire the expression of the sexual differentiation gene, doublesex; undergo doublesex-dependent programmed cell death in males; and are remodeled in females for functions in female mating behavior. Our results demonstrate that the neural circuits for courtship in Drosophila are built in part using neurons that are sexually reprogrammed from former sex-shared activities in larval life. •DDAG_C/D neurons contribute to ovipositor extrusion in adult females•The DDAG_C/D neurons are recycled embryonic-born larval neurons•DSX-M and DSF regulate DDAG_C/D neuronal survival during metamorphosis Diamandi et al. identify two female-specific interneurons that contribute to a courtship rejection behavior performed by mated Drosophila females. These neurons are present in larvae as mature, sex-shared interneurons; gain sexual identity during metamorphosis; and are recycled for reproductive activities in adult females.