Spontaneous ovulation control by ovary-to-neuron relaxin signaling in Drosophila

Ovulation enables mature oocytes to exit the ovary for potential fertilization. In Drosophila, ovulation is induced by mating but also occurs spontaneously in virgins, with rates varying widely in natural populations: short oocyte retention is ancestral, while longer retention is favored in colder climates. The molecular regulation of spontaneous ovulation remains unclear. We have found that disrupting the relaxin/insulin-like peptide Dilp8 or its receptor Lgr3 (an ortholog of vertebrate RXFP1/2) in mature follicle cells or specific neurons, respectively, delays ovulation and facilitates oogenesis progression, leading to mature follicle accumulation in the ovary. Mating largely rescues these defects, suggesting the pathway is dispensable post-mating. Dilp8-Lgr3 signaling ensures high oocyte quality in virgins by promoting elimination of lower-quality aging oocytes and by antagonizing oogenesis progression. This ovarian-nervous-system cross-talk provides a molecular basis for oocyte retention time regulation in Drosophila and supports an ancient role for relaxin-like signaling in regulating female reproductive physiology.

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