Adaptation to host plants modulates the dependence of tephritid fruit flies on their gut bacterial communities

Insect gut microbial communities are recognized as important factors facilitating insect adaptation to host plant defenses. However, the impact of co-evolution with host plants on insects’ reliance on their gut bacterial communities remains poorly understood. In this study, we first showed a decrease in fitness for Bactrocera dorsalis, Zeugodacus cucurbitae, Zeugodacus tau, and Bactrocera correcta after eliminating their gut microbes, but only when they were fed on non-preferred hosts; no significant fitness changes were observed on preferred hosts. Furthermore, after a simulated adaptation period with bitter melon feeding, Z. cucurbitae larvae, whether axenic, symbiotic, or gnotobiotic, exhibited comparable fitness levels. In contrast, axenic larvae of B. dorsalis continued to display reduced fitness compared to their symbiotic and gnotobiotic counterparts. Our findings also revealed that bacterial removal altered gene expression patterns in B. dorsalis, indicating deficiencies in nutrient acquisition, assimilation, immunity, and detoxification processes, whereas these changes were less pronounced in Z. cucurbitae. Additionally, our experiments demonstrated that, unlike Z. cucurbitae, B. dorsalis relies on its intestinal flora to significantly detoxify bitter melon toxins. These results suggest that Z. cucurbitae may have developed microbe-independent strategies, such as genetically encoded detoxification or tolerance mechanisms, to cope with toxic host challenges.