The impacts of almond pollination on honeybee viral dynamics

Seasonal aggregation of hosts can rapidly reshape microbial and viral communities, with consequences for disease dynamics and spillover risk. Each year, millions of honey bee ( Apis mellifera ) colonies experience a mass human-mediated intercontinental ‘migration’ to California’s Central Valley to pollinate most of the world’s almond supply. Clearly, this ‘mass mixing event’ with hives from across the country has the risk of spreading highly virulent pathogens, including viruses. It is essential to weigh the benefits of the almond bloom against the risks of disease in honeybees, which may also affect native pollinators. We conducted an observational longitudinal RNA-seq study of colonies from a commercial beekeeping operation before, during, and after almond pollination, compared with non-migrating control colonies. We found that viral diversity increased in honeybee colonies during and directly after the bloom; however, it returned to pre-bloom levels a month later. The virome community composition also became more uniform between hives after the bloom. Hives in closer proximity had more similar viromes. This spatial variation suggests that inter-colony drift is a potential transmission route. Together, these findings suggest that the bloom increases viral transmission, with no single virus dominating the communities. Instead, a group of viruses (black queen cell virus, Lake Sinai Virus, deformed wing virus) were responsible for community shifts. Although crop bloom increased viral diversity and community homogenization, this effect was short-lived, with viromes reverting to pre-bloom levels once hives left the orchards. These findings indicate that pollination events can transiently restructure viral communities in managed bees.