The mutualism between legumes and rhizobia is clearly the product of past coevolution. However, the nature of ongoing evolution between these partners is less clear. To characterize the nature of recent coevolution between legumes and rhizobia, we used population genomic analysis to characterize selection on functionally annotated symbiosis genes as well as on symbiosis gene candidates identified through a two-species association analysis. For the association analysis, we inoculated each of 202 accessions of the legume host Medicago truncatula with a community of 88 Ensifer meliloti strains. Multi-strain inoculation, which better reflects the ecological reality of rhizobial selection in nature than single-strain inoculation, allows strains to compete for nodulation opportunities and host resources and for hosts to preferentially form nodules and provide resources to some strains. We found extensive host by symbiont, i.e., genotype-by-genotype, effects on rhizobia fitness and some annotated rhizobia genes bear signatures of recent positive selection. However, neither genes responsible for this variation nor annotated host symbiosis genes are enriched for signatures of either positive or balancing selection. This result suggests that stabilizing selection dominates selection acting on symbiotic traits and that variation in these traits is under mutation-selection balance. Consistent with the lack of positive selection acting on host genes, we found that among-host variation in growth was similar whether plants were grown with rhizobia or N-fertilizer, suggesting that the symbiosis may not be a major driver of variation in plant growth in multi-strain contexts.

These data were collected from an experiment with 202 accessions of Medicago truncatula inoculated with a mixture of 88 strains of Ensifer (Sinorhizobium) meliloti. The frequency of each strain was estimated before inoculation and in the nodules at the end of the experiment using pooled genome sequencing. The data include association analyses (GWAS) on the differences in strain composition among host genotypes and the differences in fitness among rhizobial strains.

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