The genetic basis of cooperation and conflict in natural populations of a model symbiont

Abstract

Given the need to predict the outcomes of evolution in host-associated microbiomes, whether microbial and host fitnesses trade off, generating conflict, remains a pressing question. Examining the relationships between host and microbe fitness proxies at both the phenotypic and genomic levels can illuminate the mechanisms underlying cooperation and conflict, while addressing the challenge of measuring microbial fitness. We examined naturally-occurring genetic variation in 191 strains of the model microbial symbiont, Ensifer meliloti, paired with each of two host Medicago truncatula genotypes in single- or mixed-strain inoculation experiments to determine how multiple proxies of microbial and host fitness were related to one another and test key predictions about mutualism evolution at the ge-nomic scale. We found little evidence for fitness conflict; loci tended to have concordant effects on both microbe and host fitnesses, even in environments with multiple competing microbes. Our results emphasize the importance of quantifying microbial competitive fitness for understanding microbiome evolution and thus harnessing microbiomes to improve host fitness. Additionally, we find that mutualistic coevolution between legumes and rhizobia can act to maintain, rather than erode, genetic diversity, potentially explaining why variation in mutualism traits persists in nature.