Herbivorous insects can shape the epidemiology of disease in plants by vectoring numerous phytopathogens. While the consequences of infection are often well-characterized in the host plant, the extent...

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 symbiosis and how this diversity influences host ecology in natural populations. The aphid facultative symbiont Regiella insecticola is ideally suited to this question because of its 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. We identified a plasmid (pRILSR1) that encodes a type IV secretion system and a highly expressed predicted effector that has been convergently acquired by Regiella strains from pea aphids. Notably, only pRILSR1-bearing strains confer protection against the specialist fungal pathogen Pandora neoaphidis , indicating that gains and losses of the plasmid underlie the evolution of this key defensive phenotype. Using a multi-year field study, we further show that the pRILSR1 plasmid is strongly associated with Regiella found in pea aphid populations adapted to specific host plants, driving variation in symbiont-mediated defense across populations. Together, our results show that mobile genetic elements generate key adaptive traits in microbial symbionts and, in doing so, drive phenotypic divergence among host populations. ### Competing Interest Statement The authors have declared no competing interest.

Abstract. Carpenter ants (Family Formicidae; Genus Camponotus) are a globally distributed, arboreal clade. They harbor an intracellular obligate bacterial

Abstract. Insects ally with microbial symbionts for a diversity of services. The range of these interactions is wide, spanning from beneficial to pathogeni

Abstract. Insects ally with microbial symbionts for a diversity of services. The range of these interactions is wide, spanning from beneficial to pathogeni