On the Front Line: Quantitative Virus Dynamics in Honeybee (Apis mellifera L.) Colonies along a New Expansion Front of the Parasite Varroa destructor

Over the past fifty years, annual honeybee (Apis mellifera) colony losses have been steadily increasing worldwide. These losses have occurred in parallel with the global spread of the honeybee parasite Varroa destructor. Indeed, Varroa mite infestations are considered to be a key explanatory factor for the widespread increase in annual honeybee colony mortality. The host-parasite relationship between honeybees and Varroa is complicated by the mite's close association with a range of honeybee viral pathogens. The 10-year history of the expanding front of Varroa infestation in New Zealand offered a rare opportunity to assess the dynamic quantitative and qualitative changes in honeybee viral landscapes in response to the arrival, spread and level of Varroa infestation. We studied the impact of de novo infestation of bee colonies by Varroa on the prevalence and titres of seven well-characterised honeybee viruses in both bees and mites, using a large-scale molecular ecology approach. We also examined the effect of the number of years since Varroa arrival on honeybee and mite viral titres. The dynamic shifts in the viral titres of black queen cell virus and Kashmir bee virus mirrored the patterns of change in Varroa infestation rates along the Varroa expansion front. The deformed wing virus (DWV) titres in bees continued to increase with Varroa infestation history, despite dropping infestation rates, which could be linked to increasing DWV titres in the mites. This suggests that the DWV titres in mites, perhaps boosted by virus replication, may be a major factor in maintaining the DWV epidemic after initial establishment. Both positive and negative associations were identified for several pairs of viruses, in response to the arrival of Varroa. These findings provide important new insights into the role of the parasitic mite Varroa destructor in influencing the viral landscape that affects honeybee colonies.Author Summary: Honeybees currently face a dramatic decline worldwide. The main honeybee parasite - Varroa destructor - plays a key role in these mortalities, since uncontrolled infestation inevitably results in the death of the colony. The pathological effects of Varroa infestations are partly attributed to the association of the mite with several honeybee viruses, primarily deformed wing virus (DWV). However the exact role that Varroa plays in the spread of honeybee viruses is still unknown. The recent arrival of Varroa in New Zealand provided a timely opportunity to gain insights into the complex relationship between bees, Varroa and viruses. Our data reveal that the different viruses have unique quantitative dynamics in relation to Varroa infestation, resulting in a shifting succession of virus infections that ultimately leaves DWV as the predominant infection. Assumption-free analysis shows consistent clustering of the data according to Varroa-infestation history, confirming a progressive change in the overall virus landscape co-incident with Varroa infestation. We also highlight possible interactions between several viruses. Our findings may have implications for the beekeeping industry, by highlighting the dynamic changes in the virus infections due to the arrival of Varroa, and how these are maintained.