Tissue-specific transcriptomic analysis of accelerated reproductive development of immature Queensland fruit fly induced by raspberry ketone ingestion

Background: Raspberry ketone (RK) is a phytochemical compound that enhances male mating performance and accelerates sexual development in immature male Queensland fruit fly (Bactrocera tryoni). While the behavioural effects of RK are well established, the tissue-specific molecular responses remain unclear. We investigated how RK reshapes gene expression in a tissue-specific and time-dependent manner during sexual maturation. 

Results: We performed tissue-specific transcriptomic profiling across five key tissues, including testes, accessory gland, ejaculatory apodeme, rectal gland, and carcass, over four developmental time points (days 3, 6, 9, and 12) in RK-fed and RK-unfed males. RK ingestion induced distinct, tissue-specific transcriptional changes, with the accessory gland and ejaculatory apodeme showing the strongest responses. Differential gene expression and weighted gene co-expression network analysis revealed that, compared to unfed males, RK-fed males exhibited fewer differentially expressed genes but higher expression intensity, suggesting a focused and efficient transcriptional response. Key genes involved in spermatogenesis (dhd, opa, onecut), muscle development (act88F, flightin, zasp67), cuticle remodelling (kkv, cht7), and neuroendocrine signalling (DopEcR, DIP-delta, BOSS) were upregulated in RK-fed males. Temporal analysis showed early and mid-phase transcriptional surges across reproductive tissues, aligning with accelerated reproductive organ development and reproductive readiness. 

Conclusion: RK accelerates male sexual maturation by amplifying time-dependent transcriptional responses in reproductive tissues. The most pronounced temporal responses to RK were observed in the accessory and rectal glands. This study provides the first molecular framework to understand the effects of phytochemical ingestion on developmental timing and reproductive readiness in tephritid flies.