Blue light toxicity drives the gut microbiota-mediated lipid accumulation in Drosophila

Since the origin of life, the sunlight-driven environment on Earth has shaped the evolution of organisms. Blue light (BL), a major component of sunlight, is crucial to the biological processes of many insect species, yet excessive exposure can be highly toxic. BL toxicity can affect fitness and act as a selective pressure in insects. However, tolerance and evolutionary adaptation to this stressor remain largely unexplored. Here, we used Drosophila melanogaster as a model to select for BL tolerance over 60 generations. The selected line (SL) exhibited an obese phenotype accompanied by midgut elongation. Surprisingly, BL tolerance in the SL was dependent on gut microbiota–mediated lipid accumulation. In addition, we found that parental BL exposure plays a vital role in midgut elongation and increased abundance of beneficial bacteria. Whole-genome and transcriptome analyses consistently highlighted interactions between the microbiota and lipogenesis genes. Remarkably, manipulation of lipogenesis via these genes conferred BL tolerance even in the absence of selection. We hypothesise that the acquisition of BL tolerance occurs through ‘adaptive obesity’ by maximising the benefits of the gut microbiota. Our findings demonstrate that evolutionary adaptations to environmental stress can be driven by optimised interactions with the microbiota.