Holobiont integrity in Ceratitis capitata (Diptera: Tephritidae) enhances larval development: implications for the sterile insect technique

Abstract

All eukaryotic organisms harbour a diverse gut microbiota that supports host physiology. In tephritid fruit flies, bacteria contribute to nutrient assimilation, host defence evasion and detoxification of secondary plant compounds. The Mediterranean fruit fly, Ceratitis capitata (Wiedemann), is an economically important pest, often controlled with the sterile insect technique (SIT), which relies on the release of high-quality sterile males. While bacterial probiotic diets improve the performance of flies reared in the context of the SIT, the contribution of fungi remains largely unexplored. In this study, we evaluated the effects of microbiota disruption on C. capitata development and fitness by comparing the progeny from antimicrobial-treated (aposymbiotic) and untreated (symbiotic) flies. Eggs from both groups were inoculated into oranges, a natural host fruit for C. capitata, and offspring survival was tracked across life stages. Symbiotic progeny showed significantly higher larval recovery, egg hatch, pupation, adult emergence, and longevity compared with the aposymbiotic progeny, demonstrating that an intact microbiome is critical for successful fruit exploitation and larval development. These results are consistent with parental microbiota effects on offspring performance and suggest that maintaining the gut microbiota as a functional community supports larval development in fruit. Disruption of this community not only reduces immature survival but also compromises adult fitness, potentially undermining SIT efficiency. Probiotic strategies for mass rearing may therefore benefit from integrating both bacterial and fungal components to optimise C. capitata performance in SIT programs, while targeted studies are still needed to disentangle specific microbial contributions and identify transmission routes.