Male cuticular pheromones stimulate removal of the mating plug and promote re-mating through pC1 neurons inDrosophilafemales

Abstract

In birds and insects, females uptake sperm for a specific duration post-copulation known as the ejaculate holding period (EHP) before expelling unused sperm and the mating plug through sperm ejection. Our study uncovered that encountering males or mated females after mating substantially shortens EHP, a phenomenon we term ‘male-inducedEHPshortening (MIES)’. MIES requires Or47b+ olfactory and ppk23+ gustatory neurons, activated by 2-methyltetracosane and 7-Tricosene, respectively. These odorants raise cAMP levels in pC1 neurons, responsible for processing male courtship and regulating female mating receptivity. Elevated cAMP levels in pC1 neurons reduce EHP and reinstate their responsiveness to male courtship cues, promoting re-mating with faster sperm ejection. This study establishes MIES as a genetically tractable model of sexual plasticity with a conserved neural mechanism.Significance StatementSexual plasticity, adapting reproductive behaviors to social changes, was explored in the fruit fly, a genetically tractable model insect. Findings revealed that inseminated females, encountering another courting male post-mating, shorten the ejaculate holding period (EHP). Specific olfactory and gustatory pathways regulating this phenomenon were identified, converging on the pC1 neurons in the brain-a conserved neural circuit regulating female mating activity. Odors associated with EHP shortening increased the second messenger cAMP. The elevated cAMP transiently heightened the excitability of pC1 neurons, enabling inseminated females to promptly remove the male ejaculate and engage in the subsequent mating more readily. This study establishes a behavioral model for sexual plasticity and provide a framework for understanding the involved neural processes.