Local adaptation and maladaptation of tree populations to microbial communities across ranges
Decades of research has demonstrated that plant populations are very often locally adapted to their abiotic conditions, especially climate. However, plant fitness can be affected as much or more by interactions with complex biotic communities, including competitors, mutualists, and natural enemies, and the degree to which plant populations are locally adapted (or maladapted) to their biotic communities remains less clear. Recent evidence has demonstrated that massively diverse microbial communities in soils and roots may have particularly strong effects on plant populations and communities – however, very little is known about plant adaptation to diverse microbial communities, rather than to specific pathogens or mutualists. We tested whether seedlings of two related tree species, Carpinus caroliniana and Ostrya virginiana, performed better or worse in soil communities collected from conspecific individuals at the same site as the seed population (conspecific local), from near conspecific trees from other sites (conspecific foreign), or from near heterospecific trees at their local site (heterospecific local), in controlled conditions. Additionally, we characterized the fungal communities on tree roots and collected soils from the source sites using next-generation sequencing to gain additional insight into the patterns of adaptation.
Overall, populations performed no better or worse in their local than foreign conspecific soil communities, although both species tended to perform better in conspecific than heterospecific soil communities. However, these patterns masked more subtle evidence for adaptation and maladaptation to microbial communities. Seedlings performed better when inoculated with fungal communities that had higher compositional similarity to the fungal community present on roots of mature conspecific individuals in the source field site. However, when controlling for this effect of community similarity, seedlings inoculated with their local, conspecific microbial community significantly underperformed. This suggests that seedlings may be adapted to the higher order structure of their local microbial community (e.g. presence of certain mycorrhizal genera), but maladapted to specific microbial strains. Such a pattern may have consequences for gene flow in the face of changing climates, as genotypes may benefit from escaping local microbial strains but only if they can maintain a certain microbial community structure in their new locations.