Multi-omics reveal developmental stage-specific adaptations of Tropilaelaps mercedesae to the honeybee host.

The ectoparasitic honeybee (Apis mellifera) mite Tropilaelaps mercedesae represents a serious threat to Asian apiculture and a growing concern for global beekeeping due to its high reproductive capacity and host adaptability. However, the regulatory mechanisms underlying its host adaptation across life stages remain poorly characterized. Here, we performed integrated transcriptomic, proteomic, and metabolomic analyses of female mites at 4 key postembryonic developmental stages: protonymphs, deutonymphs, mature adults, and reproductive adults. Our multi-omics approach reveals distinct stage-specific regulatory programs. Nymphal stages exhibit coordinated activation of chitin metabolism pathways for structural growth, neuroactive ligand-receptor interactions for neural maturation, and ATP-binding cassette (ABC) transporters for detoxification. Adult maturation involves enhanced membrane dynamics, improved energy metabolism, and increased antioxidant defenses to support reproductive capacity and environmental resilience. Reproductive adults prioritize lipid metabolism and vitellogenin synthesis to fuel embryonic development. Crucially, host adaptation emerges as a critical driver of this stage-specific regulation. Additionally, multi-omics integration highlights a developmental transition from transcriptional dominance in early stages to post-transcriptional regulation in later phases. These insights provide a systems-level understanding of the physiological orchestration enabling this parasite's ecological success, while identifying valuable molecular targets for formulating more effective strategies to control this formidable pest.