Divergence in Responsiveness to Soil Biota and Mycorrhizal Partner-Specificity Between Montane Annual and Coastal Perennial Ecotypes of Yellow Monkeyflower (mimulus Guttatus)

Premise of research. Species-level variation in interactions with root-associated microbial communities has its evolutionary origins within species, where dissection of the mechanistic basis of plant divergence is also tractable. We use montane annual and coastal perennial populations (ecotypes) of Mimulus guttatus (yellow monkeyflower) to ask whether and how plant-microbe-soil interactions have diverged between populations with distinct life histories.Methodology. We characterized fungal communities in representative montane annual (Iron Mountain) and dune perennial (Florence dunes) habitats in Oregon, where previous reciprocal transplants revealed local adaptation. We then investigated how plant ecotype, microbial source, and soil origin affected plant performance and root-associated fungal communities in a full-factorial greenhouse experiment using plants, soils, and nested inocula (sterilized, filtered to remove arbuscular mycorrhizal fungi, and whole) from the two sites.Pivotal results. In the field, coastal perennial and montane annual monkeyflowers harbored distinct fungal communities, and perennial roots were enriched for mutualistic taxa relative to local soils. In the greenhouse common garden, microbial effects were largely negative (particularly in the annual ecotype), and there was no evidence of plant local adaptation to belowground conditions. However, the coastal perennial ecotype was more colonized by arbuscular mycorrhizal fungi than the montane annual ecotype, and it preferentially recruited local arbuscular mycorrhizal fungi taxa even when inoculated from the montane source.Conclusions. Our results suggest that population divergence in life history and related traits shapes plant responsiveness to soil microbes and the specificity of their associations with root endophytic fungi, such as arbuscular mycorrhizal fungi. Complex belowground effects on plant performance do not fit a simple pattern of local adaptation but may be by-products of other drivers of plant divergence. This work advances the study of heritable variation in plant-soil-microbe interactions in a model species for understanding the genomics of plant adaptation.