Host density, genetic diversity and social groups are key factors influencing pathogen transmission in wildlife populations, but their interactions remain poorly understood in insects. Islands can provide natural laboratories with distinct populations that vary in density and genetic diversity, whereby dense, genetically homogenous populations are expected to facilitate pathogen transmission. We used bumble bees to test these predictions, assessing the population structure of the two common species Bombus pascuorum and B. terrestris across island and mainland sites in the British Isles and France and testing bees for five micro-parasitic and four viral pathogens. B. pascuorum formed distinct genetic clusters on islands, with varying levels of heterozygosity and only the Isle of Arran clustering with mainland populations. B. terrestris populations were less structured, but populations on the Isle of Man and the Scilly Isles were genetically separated from other island and mainland populations while showing low heterozygosity. Colony density was similar between species and not linked to genetic diversity, but had a positive effect on the prevalence of some pathogens. Contrary to expectations, there was no protective effect of high genetic diversity, suggesting that generalist bumble bee pathogens could be more affected by host species diversity and density. Yet, within B. terrestris populations, we found that nestmates showed more similar pathogen profiles than unrelated individuals, suggesting that genetic similarity and high contact rates within nests affect pathogen prevalence in wild 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. 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 six 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.

Host density, genetic diversity and social groups are key factors influencing pathogen transmission in wildlife populations, but their interactions remain poorly understood in insects. Islands can provide natural laboratories with distinct populations that vary in density and genetic diversity, whereby dense, genetically homogenous populations are expected to facilitate pathogen transmission. We used bumble bees to test these predictions, assessing the population structure of the two common species Bombus pascuorum and B. terrestris across island and mainland sites in the British Isles and France and testing bees for five micro-parasitic and four viral pathogens. B. pascuorum formed distinct genetic clusters on islands, with varying levels of heterozygosity and only the Isle of Arran clustering with mainland populations. B. terrestris populations were less structured, but populations on the Isle of Man and the Scilly Isles were genetically separated from other island and mainland populations while showing low heterozygosity. Colony density was similar between species and not linked to genetic diversity, but had a positive effect on the prevalence of some pathogens. Contrary to expectations, there was no protective effect of high genetic diversity, suggesting that generalist bumble bee pathogens could be more affected by host species diversity and density. Yet, within B. terrestris populations, we found that nestmates showed more similar pathogen profiles than unrelated individuals, suggesting that genetic similarity and high contact rates within nests affect pathogen prevalence in wild bees.