Drivers of distance decay of host-associated microbiomes vary by host sociality and microbial association strength

Spatial patterns in microbial biodiversity can provide valuable insight into the drivers of microbial community variation; however, they are rarely explored in host-associated microbiomes, despite the significance of microbiome variation to host health and fitness. Spatial variation in animal-associated microbiomes can be influenced by several factors, including the strength of the interaction between the host and microbe (microbial association) and the likelihood of social interactions among hosts (host sociality). We investigated the processes that drive host-microbe interaction turnover in wild bees across space and found that they vary with both host sociality and microbial association. Strongly host-associated microbes in solitary bees were geographically structured by opposing processes—interaction rewiring among nearby meadows and turnover in bee species among distant meadows. The net result was that strongly host-associated interactions did not significantly vary with distance in solitary bees. In contrast, for weakly host-associated microbes in solitary bees, interaction turnover was driven solely by turnover in bee species among distant meadows, resulting in a significant relationship between similarity in host-microbe interactions and distance. For strongly host-associated microbes in social bees, networks were geographically structured, exhibiting opposing processes (rewiring among nearby meadows and turnover in both bee and microbial taxa among distant meadows). In contrast, for weakly associated microbes in social bees, networks were geographically structured solely by microbe-driven turnover, which decreased with distance. The net result was that host-microbe interactions did not significantly vary with distance in social bees. Our results demonstrate that both host sociality and host-microbial association strength can influence the drivers of spatial variation in animal-associated microbiomes.