TY - JOUR

T1 - Ancestral neural circuits potentiate the origin of a female sexual behavior in Drosophila

AU - Li, Minhao

AU - Chen, Dawn S

AU - Junker, Ian P

AU - Szorenyi, Fabianna I

AU - Chen, Guan Hao

AU - Berger, Arnold J

AU - Comeault, Aaron A

AU - Matute, Daniel R

AU - Ding, Yun

N1 - © 2024. The Author(s).

PY - 2024/10/28

Y1 - 2024/10/28

N2 - 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 endemic Drosophila species D. 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 in D. 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 circuit 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.

AB - 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 endemic Drosophila species D. 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 in D. 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 circuit 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.

KW - Animals

KW - Female

KW - Sexual Behavior, Animal/physiology

KW - Male

KW - Courtship

KW - Drosophila/physiology

KW - Wings, Animal/physiology

KW - Copulation/physiology

KW - Biological Evolution

KW - Neurons/physiology

KW - Optogenetics

KW - Neural Pathways/physiology

U2 - 10.1038/s41467-024-53610-w

DO - 10.1038/s41467-024-53610-w

M3 - Article

C2 - 39468043

VL - 15

SP - 9210

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

IS - 1

ER -