Excessive mature follicle accumulation in ovaries harms oocyte health and offspring viability. The mechanism by which females count mature follicles in their ovaries remains a mystery. Recent work demonstrated that Drosophila insulin-like peptide 8 (ILP8) is expressed in mature follicle cells but not in younger follicles. Here, we found that ILP8 is not essential for mating-induced ovulation but plays a crucial role in inducing ovulation in virgin females and preventing excessive accumulation of mature follicles. Excessive accumulation of mature follicles in ilp8-knockdown females leads to poor oocyte quality. In addition, knockdown of Lgr3 (Leucine-rich repeat-containing G protein-coupled receptor 3), encoding a previously identified ILP8 receptor, globally or neuronally showed similar ovulation/egg laying defects, accumulation of mature follicles and poor oocyte quality in virgin females. Therefore, ILP8 functions as a mature follicle sensor to prevent excessive accumulation of mature follicles and maintain oocyte quality, likely through the neuronal Lgr3 receptor in virgin females. Our findings suggest that ILP8/Lgr3 is likely essential for maintaining the optimal reproductive fitness of virgin females and for species survival in the wild, where mating success is not guaranteed.
Keywords: Ilp8; Lgr3; Mature follicle sensor; Oocyte aging; Virgin ovulation.
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