Laboratory infection experiments and field data show that emerging infectious diseases of honeybees are widespread infectious agents within the pollinator assemblage; the prevalence of deformed wing virus (DWV) and the parasite Nosema ceranae in honeybees and bumblebees is linked, and sympatric bumblebees and honeybees are infected by the same DWV strains, indicating ongoing disease transmission. Efficient pollination is vital for both crop production and ecosystem sustainability, and there is evidence to suggest that emerging infectious diseases are contributing to a decline in populations of some important insect pollinators. This study combines laboratory infection experiments and field studies to demonstrate infectivity of two serious honeybee (Apis mellifera) pathogens in a wild pollinator, the bumblebee (Bombus terrestris). Data from across the United Kingdom show that there is co-localization of deformed wing virus (DWV) and the microsporidian parasite Nosema ceranae in the two types of pollinator, and that the honeybee disease can be infectious in bumblebees. This work indicates that wild pollinator populations may be at risk, and unlike managed populations of Apis, they are not protected by intervention from beekeepers. Such a loss of wild pollinators would significantly decrease crop pollination efficiency. Emerging infectious diseases (EIDs) pose a risk to human welfare, both directly1 and indirectly, by affecting managed livestock and wildlife that provide valuable resources and ecosystem services, such as the pollination of crops2. Honeybees (Apis mellifera), the prevailing managed insect crop pollinator, suffer from a range of emerging and exotic high-impact pathogens3,4, and population maintenance requires active management by beekeepers to control them. Wild pollinators such as bumblebees (Bombus spp.) are in global decline5,6, one cause of which may be pathogen spillover from managed pollinators like honeybees7,8 or commercial colonies of bumblebees9. Here we use a combination of infection experiments and landscape-scale field data to show that honeybee EIDs are indeed widespread infectious agents within the pollinator assemblage. The prevalence of deformed wing virus (DWV) and the exotic parasite Nosema ceranae in honeybees and bumblebees is linked; as honeybees have higher DWV prevalence, and sympatric bumblebees and honeybees are infected by the same DWV strains, Apis is the likely source of at least one major EID in wild pollinators. Lessons learned from vertebrates10,11 highlight the need for increased pathogen control in managed bee species to maintain wild pollinators, as declines in native pollinators may be caused by interspecies pathogen transmission originating from managed pollinators.

Methods are described for working with Nosema apis and Nosema ceranae in the field and in the laboratory. For fieldwork, different sampling methods are described to determine colony level infections at a given point in time, but also for following the temporal infection dynamics.

Adult honey bees are maintained in vitro in laboratory cages for a variety of purposes.

Summary: Declining populations of bee pollinators are a cause of concern, with major repercussions for biodiversity loss and food security.RNAviruses associated with honeybees represent a potential threat to other insect pollinators, but the extent of this threat is poorly understood. This study aims to attain a detailed understanding of the current and ongoing risk of emerging infectious disease (EID) transmission between managed and wild pollinator species across a wide range ofRNAviruses. Within a structured large‐scale national survey across 26 independent sites, we quantify the prevalence and pathogen loads of multipleRNAviruses in co‐occurring managed honeybee (Apis mellifera) and wild bumblebee (Bombusspp.) populations. We then construct models that compare virus prevalence between wild and managed pollinators. MultipleRNAviruses associated with honeybees are widespread in sympatric wild bumblebee populations. Virus prevalence in honeybees is a significant predictor of virus prevalence in bumblebees, but we remain cautious in speculating over the principle direction of pathogen transmission. We demonstrate species‐specific differences in prevalence, indicating significant variation in disease susceptibility or tolerance. Pathogen loads within individual bumblebees may be high and in the case of at least oneRNAvirus, prevalence is higher in wild bumblebees than in managed honeybee populations. Our findings indicate widespread transmission ofRNAviruses between managed and wild bee pollinators, pointing to an interconnected network of potential disease pressures within and among pollinator species. In the context of the biodiversity crisis, our study emphasizes the importance of targeting a wide range of pathogens and defining host associations when considering potential drivers of population decline.

Emerging infectious diseases (EIDs) have contributed significantly to the current biodiversity crisis, leading to widespread epidemics and population loss. Owing to genetic variation in pathogen virulence, a complete understanding of species decline requires the accurate identification and characterization of EIDs. We explore this issue in the Western honeybee, where increasing mortality of populations in the Northern Hemisphere has caused major concern. Specifically, we investigate the importance of genetic identity of the main suspect in mortality, deformed wing virus (DWV), in driving honeybee loss. Using laboratory experiments and a systematic field survey, we demonstrate that an emerging DWV genotype (DWV-B) is more virulent than the established DWV genotype (DWV-A) and is widespread in the landscape. Furthermore, we show in a simple model that colonies infected with DWV-B collapse sooner than colonies infected with DWV-A. We also identify potential for rapid DWV evolution by revealing extensive genome-wide recombination in vivo . The emergence of DWV-B in naive honeybee populations, including via recombination with DWV-A, could be of significant ecological and economic importance. Our findings emphasize that knowledge of pathogen genetic identity and diversity is critical to understanding drivers of species decline.