Phenotypic divergence is driven by mobile genetic elements in a heritable insect symbiont

Heritable microbes profoundly influence insect biology, yet the traits they confer often evolve rapidly and differ among closely related symbiont strains. Despite their importance, we lack a clear understanding of how novel traits arise in symbionts and how this diversity influences host ecology in nature. The aphid facultative symbiont Regiella insecticola is ideally suited to address this question due to strong lineage-specific variation in host benefits. By generating 20 high-quality genomes, we found that Regiella's evolution is driven largely by gene gains mediated by mobile genetic elements (MGEs). A plasmid (pRILSR1) encoding a type IV secretion system and a highly expressed predicted effector has spread horizontally between distantly related Regiella clades associated with pea aphids. Notably, only pRILSR1-bearing strains confer protection against the fungal pathogen Pandora neoaphidis. Moreover, loss of the plasmid by a protective strain in culture resulted in the loss of protection, indicating that pRILSR1 is required for the defensive phenotype. In a multiyear field study, pRILSR1 frequency varied systematically among host plant-associated pea aphid populations and predicted differences in symbiont-mediated fungal resistance. Together, our results show that gain and loss of a single MGE contributes to divergence in a key adaptive trait, providing a mechanism by which symbiont evolution generates phenotypic differences among host populations.