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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.

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