Ecological genomics of mutualism decline in response to nitrogen fertilization

Background/Question/Methods

Mutualisms are ubiquitous in nature and play critical roles in natural ecosystems. The benefits of mutualism are well-known to depend on the environmental context, leading to predictions that mutualisms might break down in the face of anthropogenic changes. Changes in keystone mutualisms might be an important consideration in predicting ecosystem responses to environmental change. Worldwide elevated nitrogen inputs resulting from human activities are causing profound ecological changes in diverse ecosystems, but the evolutionary consequences are not as well known. Increased nitrogen inputs have been hypothesized to drive the evolution of decreased benefits in the legume-rhizobium mutualism, in which rhizobial bacteria trade fixed nitrogen in exchange for photosynthates from legume hosts. Because of their importance in natural and managed ecosystems, decline in legume-rhizobium mutualisms could have important consequences for the ecosystem processes to which these interactions contribute. We have used common garden experiments, molecular population genomics, and mesocosms to study how nitrogen fertilization affects the evolution of this important mutualism and whether evolutionary effects might scale up to the community and ecosystem levels.

Results/Conclusions

Using a long-term (22 year) nitrogen addition experiment, we have used quantitative genetic and phylogenetic approaches to demonstrate that rhizobium partner quality (benefit to the plant host) has declined in response to elevated nitrogen inputs, and that this is an evolutionary response. Using population genomic analyses of 63 rhizobium strains from nitrogen-evolved and control populations, we have found that genetic differentiation at a key symbiosis gene region on the symbiotic plasmid (pSym) has contributed to this decline of partner quality, and moreover that patterns of genetic variation at selected loci were consistent with recent positive selection within nitrogen-fertilized environments. In mesocosm experiments that included clover hosts as well as other non-legume members of the plant community, we found that nitrogen-evolved rhizobium populations led to decreased soil nitrogen pools and shifts in plant community composition. Together our results suggest that, as predicted by theory, the evolutionary trajectories of resource mutualisms such as the legume-rhizobium symbiosis are indeed sensitive to environmental changes. Moreover these evolutionary changes can feed back to influence the larger communities and ecosystems in which mutualisms occur.