Matched Fruit-Larva Metabolomics Identifies Host-Associated Metabolic Signatures After Multi-Generational Laboratory...

Zeugodacus tau (Walker) is a polyphagous invasive tephritid capable of cross-family host shifts from ancestral Cucurbitaceae crops to phylogenetically divergent commercial fruits, causing severe horticultural economic losses. As an obligate fruit-boring pest, Z. tau largely relies on larval metabolic plasticity to achieve successful colonization of novel hosts during host shifts. However, few matched fruit-larva metabolomic studies integrate host chemistry to larval physiology, hindering sustainable pest control development. We performed untargeted LC-MS metabolomics on matched fruit and third-instar larval samples from eight hosts after multi-generational acclimation. Principal component analysis (PCA) split fruit and larval metabolomes into cucurbit and non-cucurbit clusters, indicating that larval metabolic profiles align with host fruit chemistry during host shifts. Cucurbit fruits contained uniformly high γ-aminobutyric acid (GABA), and their larvae exhibited enriched glutamate (Glu)-centred amino acid pathways. Non-cucurbit fruits showed heterogeneous chemical composition: larvae-fed banana, mango and pitaya all possessed high UDP-glucose (UDPG), whose levels correlated with fruit glucose-6-phosphate (G6P) enriched in banana and mango. Overall, larvae colonizing distinct non-cucurbit hosts deployed a suite of divergent carbohydrate metabolic modules to respond to variable fruit chemical microenvironments. Banana and pitaya larvae showed enhanced starch-sucrose turnover, whereas mango larvae featured prominent ascorbate and aldarate metabolism; both pathways are closely connected to carbohydrate homeostasis. Orange and guava larvae activated distinct gluconeogenic branches. Gluconeogenesis itself constitutes an important component of carbohydrate metabolism. This dual-metabolome profiling uncovered host-specific biomarkers and two divergent metabolic strategies underlying the host shift in Z. tau, characterizing host-linked metabolic variation after long-term laboratory acclimation, which delivers correlative biochemical clues for subsequent pest management research.