Bumble Bees and Honey Bees on Islands Harbour Reduced Viral Species Richness, Yet Honey Bee Populations Are Dominated by a Deformed Wing Virus Recombinant

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. Here 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 bees harbour a distinct viral community that was not affected by varroa but geographically structured. In honey bees, however, varroa-present populations contained more viral reads driven by a high abundance of deformed wing virus (DWV). Within the 6 years between the sampling events, DWV underwent a shift from mostly DWV-B towards a mix of DWV-B and 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.