PS 35-146
Widespread negative frequency-dependent selection found in the legume/rhizobia symbiosis could maintain microbial diversity
The origin and maintenance of microbial diversity depends on negative frequency-dependent selection (FDS), where rare variants in a population produce more offspring than common ones. Current explanations for the diversity of strategies in mutualisms posit specialization between partners in a spatial context, context dependence in terms of genotype or environment dependent fitness, or high mutation rate of signals to generate negative FDS. In the legume/rhizobia mutualism, a rhizobium that forms a nodule typically produces 10^5 to 10^6 offspring, a large fitness benefit. To measure FDS in the legume/rhizobia symbiosis, we performed a meta-analysis of experiments that manipulated inoculum ratios of competing strains to find the final nodule ratios of those strains.
For each experiment in the literature, we plotted the log inoculum ratio against the log nodule ratio of the strains and found the slope of that relationship. With no frequency dependent selection the slope is 1, positive frequency dependent selection generates slopes greater than 1, and negative frequency dependence produce slopes less than 1. We analyzed 146 experiments from 31 papers. We used a mixed-model approach to assess the influence of covariates such as nodule type, plant genus, and strain relatedness on the strength of negative FDS.
Results/Conclusions
Across the 146 experiments performed by different labs with different strains and legume species, the rarer rhizobium strain founded more nodules than expected based on its competitive ability at a 1:1 inoculum ratio. The mean slope was 0.51, substantially less than the predicted slope of 1 when no frequency-dependence is present (p < 2e-16). Biologically, this means that when one of two equally competitive strains makes up only 1% of the inoculum, it generates almost 10% of the plant’s nodules. When two competing strains were near-isogenic, such as when one strain was an antibiotic-resistant mutant of the other, negative FDS surprisingly still occurred but was not as strong. All twelve plant genera featured in our dataset demonstrated negative FDS in nodule formation. Other covariates, which were system sterility, inoculum density, marker type, nitrogen fixation, and nodule type, could not be shown to affect FDS. We found that the degree of frequency-dependence was unrelated to the strains’ relative competitiveness (p=.80). While the theoretical implications of negative FDS are relatively well understood, the biological basis of this phenomenon in legumes is unclear and has profound implications for our understanding of co-evolutionary dynamics between rhizobia and their legume hosts.