Ancestral neural circuits potentiate the origin of a female sexual behavior

Abstract

Courtship interactions are remarkably diverse in form and complexity among species. How neural circuits evolve to encode new behaviors that are functionally integrated into these dynamic social interactions is unknown. Here we report a recently originated female sexual behavior in the island endemicDrosophilaspeciesD. santomea, where females signal receptivity to male courtship songs by spreading their wings, which in turn promotes prolonged songs in courting males. Copulation success depends on this female signal and correlates with males’ ability to adjust his singing in such a social feedback loop. Functional comparison of sexual circuitry across species suggests that a pair of descending neurons, which integrates male song stimuli and female internal state to control a conserved female abdominal behavior, drives wing spreading inD. santomea. This co-option occurred through the refinement of a pre-existing, plastic circuit that can be optogenetically activated in an outgroup species. Combined, our results show that the ancestral potential of a socially-tuned key circuit node to engage the wing motor program facilitates the expression of a new female behavior in appropriate sensory and motivational contexts. More broadly, our work provides insights into the evolution of social behaviors, particularly female behaviors, and the underlying neural mechanisms.

Comparative connectomics of the descending and ascending neurons of theDrosophilanervous system: stereotypy and sexual dimorphism

“…7h,i), suggesting that there might be a female wing phenotype that has not yet been described experimentally. This is reminiscent of recent observations that vpoDN may control a wing-spreading behaviour in the evolutionarily related Drosophilid D. santomea (Li et al, 2023). The only common downstream target of DNp13 in males and females, with a 2% threshold, is IN12A002 (Fig.…”