Interspecific conflict and the evolution of ineffective rhizobia

Abstract

Microbial symbionts exhibit broad genotypic variation in their fitness effects on hosts, leaving hosts vulnerable to costly partnerships. Interspecific conflict and partner‐maladaptation are frameworks to explain this variation, with different implications for mutualism stability. We investigated the mutualist service of nitrogen fixation in a metapopulation of root‐nodule forming Bradyrhizobium symbionts in Acmispon hosts. We uncovered Bradyrhizobium genotypes that provide negligible mutualist services to hosts and had superior in planta fitness during clonal infections, consistent with cheater strains that destabilise mutualisms. Interspecific conflict was also confirmed at the metapopulation level – by a significant negative association between the fitness benefits provided by Bradyrhizobium genotypes and their local genotype frequencies – indicating that selection favours cheating rhizobia. Legumes have mechanisms to defend against rhizobia that fail to fix sufficient nitrogen, but these data support predictions that rhizobia can subvert plant defenses and evolve to exploit hosts.

No selection for cheating in a natural meta‐population of rhizobia

“…Selection for cheating should manifest as a negative genetic covariance between an organism’s fitness and its quality as a mutualist, measured as the organism’s effect on its partner’s fitness (Friesen, ; Porter & Simms, ; Jones et al, ). Gano‐Cohen et al () conclude that rhizobia cheat based on finding a negative correlation between rhizobium fitness and symbiotic effectiveness (see their Fig. 5).…”

“…Gano‐Cohen et al () then used sequence data from a previous study to estimate strain frequencies at the field sites where the bacteria were collected. They report the frequencies of Bradyrhizobium chromosomal (CHR) and ‘symbiosis island’ (SI) haplotypes within each population.…”

“…I downloaded their data (Gano‐Cohen et al, ) and discovered that for the population where strains 155 and 156 were sampled (YUC; Fig. ), genotype frequencies were calculated from just two (SI frequencies) or seven (CHR frequencies) plants.…”

“…Each blue line is a regression line resulting from sampling the same numbers of nodules at random from each population; randomization data points not shown. Data from Gano‐Cohen et al ().…”

“…One hundred times per population, I randomly chose two or four plants from each population to calculate SI and CHR genotype frequencies, respectively. These were the minimum number of plants used to calculate genotype frequencies in Gano‐Cohen et al (). I then averaged genotype frequencies across iterations.…”