Soil-derived, gut-dominant generalist bacteria shape the fitness of folivorous larvae.

Whether Lepidoptera harbor a conserved core gut microbiome has long remained contentious. Through large-scale microbiome profiling of folivorous larvae, their host plants, and associated soils across three climatically distinct regions of China, we identify two soil-derived generalist bacteria, Ralstonia insidiosa and Delftia sp., that colonize 97.92% of larval species examined, attaining mean relative abundances exceeding 47%, with the soil microbial reservoir as their principal source. Strikingly, these two taxa exhibit strong mutual exclusion within the larval gut yet govern host development through diametrically opposed metabolic strategies: R. insidiosa promotes larval weight gain, whereas Delftia sp. suppresses growth. This functional bifurcation, in which two widespread generalists exert opposite phenotypic effects, represents a previously undescribed phenomenon in insect-microbe symbiosis. Our findings provide broad evidence that soil microbial reservoirs can shape aboveground herbivore fitness via horizontally acquired bacteria, offering mechanistic insights for microbiome-based ecological management.