Rapid adaptive response of population fitness of Zeugodacus tau during host shifts and implications for integrated pest management strategies

Abstract

BACKGROUND: The polyphagous fruit fly Zeugodacus tau Walker (Diptera: Tephritidae) poses significant phytosanitary threats to tropical agroecosystems because of its broad host range and adaptive plasticity. Understanding the mechanisms underlying its rapid host adaptation is critical for developing sustainable integrated pest management (IPM) strategies. METHODS: We used age-stage, two-sex life table analyses coupled with untargeted metabolomics to systematically evaluate the effects of host shifts among three key host plants—luffa (Cucurbitaceae; Luffa acutangula), mango (Anacardiaceae; Mangifera indica), and bitter gourd (Cucurbitaceae; Momordica charantia)—on the developmental fitness and metabolic shifts of Z. tau. RESULTS: Zeugodacus tau exhibited a distinct intrinsic rate of increase (r), with L. acutangula being the most favored host (r = 0.0914 ± 0.0038), followed by Momordica charantia (0.0785 ± 0.0011) and Mangifera indica (0.0685 ± 0.0038). Remarkably, host-shifted populations achieved demographic stability within two generations, accompanied by rapid recovery of fecundity and host-specific metabolic adjustments, particularly in energy-related pathways (e.g., amino acid metabolic pathways). CONCLUSION: This study identifies Z. tau as an invasive pest with exceptional adaptive capacity driven by metabolic plasticity. Our findings underscore the necessity of incorporating host plant rotation and resistant cultivar deployment in IPM frameworks to disrupt its adaptive cycles. © 2025 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.