Plant-pollinator mutualisms are essential to maintain biodiversity, but anthropogenic changes are causing their rapid decline. While diverse pollinators are supported by spatially heterogenous landscapes, understanding how pollinators spill over across habitats to maintain mutualisms is an emerging research area. Theoretical models of mutualisms often ignore such cross-habitat spillover. We ask: does cross-habitat spillover maintain mutualisms and populations of mutualists? To address this gap, we demonstrate how foundational concepts from spatial ecology—metacommunities and resource subsidies—can strengthen mutualistic theory. This Perspective paper advances a novel, conceptual framework for elucidating how spillover across ecological boundaries affects mutualistic diversity, structure, function, and dynamics. Using a classic Lotka-Volterra model, we demonstrate how spatial concepts can integrate into mutualistic theory. While we focus on plant-pollinator mutualisms due their conservation relevance, we suggest questions for future work that could be extended to other types of mutualisms. Themes for future research include examining how additional community interactions and anthropogenic changes drive how spillover affects mutualisms. Ultimately, we recommend deeper integration of niche-based theory with metacommunity and resource-subsidy dynamics in the study of mutualisms.

We took advantage of a five-decade ‘chronosequence’ of host-microbiome evolution to examine changes in the gut microbiome as wild populations evolve. In an iconic example of rapid evolution in the wild, Trinidadian guppies have displayed parallel phenotypic convergence when translocated six times from high predation (HP) to low predation (LP) environments, but changes in microbiome are unknown. We find microbiomes of fish translocated 5-6 years ago were already more similar to LP native populations than HP sources, and attribute this to both environmental and host-morphological changes. While diet was a minor driver of microbiome structure, we suggest a nutritional role for the gut microbiome in guppy evolution whereby nitrogen-fixing bacteria supplement the low-nutrient diet in LP environments. We show that environment and rapid phenotypic shifts in gut traits interact to control microbiome assembly, and suggest the gut microbiome plays an important but not necessarily consistent role in rapid host evolution.