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

Abstract

Human agriculture has always raced against insect adaptation, requiring updated pest control methods and knowledge of evolutionary processes. Excessive exposure to blue light (BL) kills a wide range of insect species and has attracted attention as an alternative to chemical pesticides. Here, to understand how insects adapt to BL toxicity, we investigated evolutionary responses to BL toxicity in Drosophila melanogaster over 70 generations using laboratory selection experiments. The selected line exhibited an obese phenotype accompanied by midgut elongation, with BL tolerance dependent on gut microbiota- mediated lipid accumulation. Whole-genome and transcriptome analyses consistently highlighted interactions between the microbiota and host lipid metabolism-related genes. Remarkably, manipulating genes associated with lipid accumulation conferred BL tolerance even in the absence of selection. We suggest that the acquisition of BL tolerance occurs through adaptive obesity. Our study introduces a mechanism of evolutionary adaptation of insects against BL-based selective pressure by maximising the benefits from the gut microbiota via midgut elongation. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=141 SRC="FIGDIR/small/608892v5_ufig1.gif" ALT="Figure 1"> View larger version (62K): org.highwire.dtl.DTLVardef@111c9d5org.highwire.dtl.DTLVardef@d9bf7forg.highwire.dtl.DTLVardef@1ab46fborg.highwire.dtl.DTLVardef@1c111cd_HPS_FORMAT_FIGEXP M_FIG C_FIG Brief summaryLaboratory selection for tolerance to blue light toxicity in Drosophila revealed that gut microbiota-mediated obesity, marked by midgut elongation and increased beneficial bacteria, is a key evolutionary adaptation.