An ovarian insulin-like peptide specifically regulates energy allocation and oocyte development in...

Insects exhibit remarkable resilience and maintain high levels of reproduction despite frequently encountering nutritional restriction. However, the mechanisms governing their adaptive reproductive strategies under nutrition-restricted conditions remain poorly understood. The German cockroach Blattella germanica, a widespread urban pest, exhibits remarkable reproductive capabilities even in domestic environments where food resources are frequently limited.

In this study, we demonstrate that the ovary plays a crucial role in promoting vitellogenin biosynthesis and oocyte development under nutrition-restricted conditions through hemiovariectomy. Employing transcriptome analysis, RNAi screening, and fluorescence in situ hybridization, we identified an ovarian-enriched insulin-like peptide gene (BgILP2) that is dramatically upregulated during low nutrition conditions. Repression of BgILP2 impairs vitellogenesis in the fat body through downregulation of p-AKT and p-ERK levels while simultaneously disrupting juvenile hormone synthesis, ultimately leading to delayed oocyte development under nutrient restriction. Furthermore, under low-nutrient conditions, repression of BgILP2 led to elevated circulating sugar levels, reduced lipid and glycogen storage, and a modest increase in the lifespan of female cockroaches.

The ovarian-enriched BgILP2 responds to nutritional stress and activates the insulin signaling pathway to sustain oocyte development under nutrient-restricted conditions. Furthermore, BgILP2 mediates energy allocation and prioritizes reproductive investment potentially at the expense of longevity, which reflects a tradeoff between reproduction and somatic maintenance under nutrient restriction. These findings provide novel insights into the molecular mechanisms and adaptive strategies that enable cockroaches to maintain reproductive success in food-limited environments.