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

BACKGROUND

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.

RESULTS

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.

CONCLUSIONS

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.