Multi-Omics Analysis Reveals Coordinated Adaptations in Genes, Metabolism, and Gut Microbiota Underpinning Herbivory...

Herbivorous insects are among the most ecologically successful animal groups. However, the adaptive mechanisms that allow them to exploit plant hosts, which are often nutrient-poor (low in simple sugars, high in structural carbohydrates) and defended by toxic secondary metabolites, are not fully resolved. Here, we investigated the evolutionary basis of herbivory in Lordiphosa clarofinis, a drosophilid species feeding on living plant tissues, using multi-omics approaches. Behavioral experiments revealed a strong oviposition preference for Galinsoga parviflora (a host rich in secondary metabolites), accompanied by elevated expression of chemosensory genes linked to host discrimination. Comparative genomic analyses revealed lineage-specific expansions of gene families associated with detoxification (e.g., cytochrome P450s) and carbohydrate metabolism, alongside positive selection on genes involved in fatty acid utilization and glycogen synthesis. Transcriptomic data showed differential expression of energy metabolism pathways in response to low-sugar plant diets, with upregulation of genes linked to lipid oxidation and gluconeogenesis. Metagenomic profiling of gut microbiota identified key taxa (e.g., Bacteroidetes) capable of degrading plant polysaccharides and synthesizing essential vitamins, potentially complementing host nutritional intake. Our results demonstrate that herbivory in L. clarofinis is associated with coordinated genomic, transcriptional, and microbial changes, rather than being attributable to a single adaptive mechanism. This study highlights how multi-level biological features covary with plant-based feeding and provides a framework for investigating the complex evolutionary and ecological correlates of herbivory in insects.