Matched Fruit–Larva Metabolomics Identifies Host-Associated Metabolic Signatures After Multi-Generational Laboratory Acclimation in Zeugodacus tau (Tephritidae: Diptera)

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.