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Abstract Multicellular organisms host a rich assemblage of associated microorganisms, collectively known as their “microbiomes.” Microbiomes have the capacity to influence their hosts’ fitnesses, but the conditions under which such influences contribute to evolution are not clear. This is due in part to a lack of a comprehensive theoretical framework for describing the combined effects of host and associated microbes on phenotypic variation. Here, we address this gap by extending the foundations of quantitative genetic theory to include host-associated microbes, as well as alleles of hosts, as factors that explain quantitative host trait variation. We introduce a way to partition host-associated microbiomes into components relevant for predicting a microbiome-mediated response to selection. We then apply our general framework to a simulation model of microbiome inheritance to illustrate principles for predicting host trait dynamics, and to generalize classical narrow- and broad-sense heritabilities to account for microbial effects. We demonstrate that microbiome-mediated responses to host-level selection can arise from various transmission modes, not solely vertical, but that the contribution of non-vertical modes can depend strongly on host life history. Our work lays a foundation for integrating microbiome-mediated host variation and adaptation into our understanding of natural variation. 

Abstract Increasing warming and drought severity are projected for the Pacific Northwest (PNW) and are expected to negatively impact species composition and ecosystem function. In this study, we test the hypothesis that the impact of climatic stress (i.e., experimental warming and drought) on PNW grasslands are mediated by interactions between plant functional diversity and soil biogeochemical processes, including symbiotic nitrogen (N) fixation in legumes and free‐living asymbiotic nitrogen fixation (ANF) by soil microorganisms. To test this hypothesis, we measured the response of plants and soils to three years of warming (+2.5°C) and drought (−40% precipitation) in field experiments replicated at three different sites across a ∼520‐km latitudinal gradient. We observed interactive effects of warming and drought on functional diversity and soil biogeochemical properties, including both positive and negative changes in ANF. Although direct measurements of symbiotic nitrogen fixation (SNF) rates were not conducted, the observed variations in ANF, in conjunction with changes in legume cover, suggest a compensatory mechanism that may offset reductions in SNF. Generally, high ANF rates coincided with low legume cover, suggesting a connection between shifts in species composition and N cycling. Our ANF estimates were performed using isotopically labeled dinitrogen (¹⁵N₂) in tandem with soil carbon (C), phosphorus (P) and iron (Fe), pH, and moisture content. Along the latitudinal drought severity gradient, ANF rates were correlated with changes in species composition and soil N, P, moisture, and pH levels. These results highlight the importance of soil‐plant‐atmosphere interactions in understanding the impacts of climatic stress on ecosystem composition and function.