Host plant phylogeny predicts arbuscular mycorrhizal fungal communities, but plant life history and fungal genetic change predict feedback

Symbioses exert strong influence on host phenotypes; however, benefits from symbionts can increase or degrade over time. Understanding the context-dependence of reinforcing or degrading dynamics is pivotal to predicting stability of symbiotic benefits. Host phylogenetic relationships and host life history traits are two candidate axes that have been proposed to structure symbioses. However, the relative influence of host evolutionary history and life history on symbiont composition, and whether changes in symbiont composition translate into stronger mutualistic benefits is unknown. We tested the influence of plant phylogenetic relationships and plant life history on the composition of arbuscular mycorrhizal (AM) fungi, perhaps the most ancestral and influential of plant symbionts, and then tested whether AM fungal differentiation resulted in improved mutualism as expected from coadaptation. We constructed mycobiomes composed of seven AM fungal isolates derived from tallgrass prairie and grew them for two growing seasons with 38 grassland plant species. We found that host phylogenetic structure was a significant predictor of the composition of AM fungal communities and the genetic composition of AM fungal species, patterns consistent with phylosymbiosis. However, the phylogenetic structure of AM fungi failed to translate to improved benefits to their host. While AM fungi generally improved plant growth and mycorrhizal feedback was generally positive, the strength of feedback was not predicted by plant phylogenetic distance. The composition of the AM fungal community and genetic composition within AM fungal species were also significantly influenced by plant life history and feedbacks between early and late successional species were generally positive. Interestingly, positive mycorrhizal feedback was predicted by changes in genetic composition of the two most abundant AM fungal species, not by changes in species composition. Positive mycorrhizal feedbacks across life history can mediate plant species turnover during succession and suggests that consideration of mycorrhizal dynamics could improve ecosystem restoration.