Simultaneous adaptation and maladaptation of tree populations to local rhizosphere microbial communities at different taxonomic scales

Abstract

Plant populations are often adapted to their local conditions, but the specific selective forces creating this adaptation are often unclear. All plants interact with diverse microbial communities, but we know little about how these microbial communities as a whole shape the evolutionary trajectory of plant populations. We tested whether tree populations were adapted or maladapted to their local rhizosphere microbial communities by growing seedlings sourced from multiple locations with soil microbial communities from all locations in a fully reciprocal design, using seedling growth as a proxy for fitness. In addition, we compared the microbial composition of the experimental inocula with that of the communities we detected associating with naturally occurring trees at the seedling source populations. We found that seedlings grew similarly when inoculated with local vs foreign microbial communities, but this neutral response derived from conflicting patterns – plant populations appeared to be adapted to the presence or absence of whole taxonomic groups in their local microbial community, but were simultaneously maladapted to the particular microbial populations present in their local site. As rapid climate change and other factors push tree populations into new areas, the successful establishment of seedlings may depend critically on the balance between the novelty and familiarity of the microbial communities they encounter.