Abstract
<jats:p>Mutualisms play critical roles in organismal stress tolerance; yet environmental stressors may simultaneously alter the evolution of the mutualism itself. Stress may have particularly strong impacts on the evolution of microbial mutualists due to their capacity for rapid genetic change. Here we used a legume-rhizobia mutualism, in which plants exchange carbon for symbiotically fixed nitrogen, to evaluate how mutualisms evolve in response to stressors. We experimentally evolved populations of Rhizobium leguminasarum in a full factorial design, manipulating drought and nitrogen. We quantified genomic changes in Rhizobium populations as well as their quality as partners with their plant host, Trifolium repens. Drought selected for context-dependent stress benefits to the host; drought-adapted Rhizobium strains provided increased benefits to the host under drought, but fewer benefits to the host in well-watered environments. Conversely, nitrogen fertilization selected for decreased Rhizobium partner quality. Comparative genomics indicated that selection on standing structural variants along the symbiotic plasmid may underpin these drought benefits, specifically along genes associated with desiccation tolerance. These results suggest that stress can expand the benefits rhizobia provide to their legume hosts beyond nitrogen fixation, with rapid symbiont evolution an engine in promoting adaptive plant phenotypes.</jats:p>