Host and parasite ecology drive differences in virome composition in managed honey bees and wild bumble bees

Pollinators harbour diverse RNA viromes that play a vital role in their health. Yet, factors that shape viral communities are often unclear. The European honey bee ( Apis mellifera ) is experiencing a viral epidemic since the emergence of the parasitic mite Varroa destructor (varroa) introduced vector-borne transmission, which has also been linked to increased viral spillover into wild pollinator communities. Varroa-free island populations provide natural laboratories to study the effect of varroa, while also allowing us to ask how islands affect viral communities. Barriers that restrict the dispersal of wild pollinators and their pathogens to islands may be overcome by human-mediated transport in managed honey bees. In this study, we used islands with and without varroa and matched mainland populations of honey bees ( A. mellifera ) and bumble bees ( Bombus terrestris ) from 2015 and 2021 to explore how varroa presence and island location affect the virome of managed and wild bees. We find lower viral richness on islands in both species. Bumble bee viromes were not affected by varroa and showed a distinct community that was geographically structured. In honey bees, however, viral abundance was more evenly distributed on varroa-free islands but dominated by deformed wing virus (DWV) in varroa-present populations. Within the six years between the sampling events, DWV underwent a shift from DWV-B towards recombinant strains. Surprisingly, these shifts appeared independent of varroa. Viewing pollinator virome composition within an ecological framework provides valuable insights into the barriers to virus spread and could help to predict drivers of disease emergence.