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ABSTRACT As environments worldwide change at unprecedented rates during the Anthropocene, understanding context dependency—how species interactions vary depending on environmental context—is crucial. Combining comparative genomics across 42 angiosperms with transcriptomics, genome‐wide association mapping and gene duplication origin analyses, we show for the first time that gene family expansions are important to context‐dependent regulation of species interactions. Gene families expanded in mycorrhizal fungi‐associating plants display up to 200% more context‐dependent gene expression and double the genetic variation associated with mycorrhizal benefits to plant fitness. Moreover, we discover these gene family expansions arise primarily from tandem duplications with > 2‐times more tandem duplications genome‐wide, indicating gene family expansions continuously supply genetic variation, allowing fine‐tuning of context dependency in species interactions throughout plant evolution. Taken together, our results spotlight how widespread gene duplications can provide molecular flexibility required for plant–microbial interactions to match changing environmental conditions. 

ABSTRACT Microorganisms underpin numerous ecosystem processes and support biodiversity globally. Yet, we understand surprisingly little about what structures environmental microbiomes, including how to efficiently identify key players. Microbiome network theory predicts that highly connected hubs act as keystones, but this has never been empirically tested in nature. Combining culturing, sequencing, networks and field experiments, we isolated ‘central’ (highly connected, hub taxa), ‘intermediate’ (moderately connected), and ‘peripheral’ (weakly/unconnected) microbes and experimentally evaluated their effects on soil microbiome assembly during early succession in nature. Central early colonisers significantly (1) enhanced biodiversity (35%–40% richer communities), (2) reshaped trajectories of microbiome assembly and (3) increased recruitment of additional influential microbes by > 60%. In contrast, peripheral microbes did not increase diversity and were transient taxa, minimally affected by the presence of other microbes. This work elucidates fundamental principles of network theory in microbial ecology and demonstrates for the first time in nature that central microbes act as keystone taxa.