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

Abstract

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.

Multiyear survey targeting disease incidence in US honey bees

“…Varroa levels were significantly elevated in bees positive for both ABPV (Figure 7) and DWV (Figure 8), highlighting the role of Varroa as viral vectors (Ball and Allen 1988;Bowen-Walker et al 1999;Mondet et al 2014). ABPV has long been associated with increased honey bee mortality in mite-infested colonies (Ball and Allen 1988).…”

Honey Bee Deformed Wing Virus Structures Reveal that Conformational Changes Accompany Genome Release

“…There are concerns about the decline in populations of managed honey bees observed since 2006 (3). Often, this decrease in honey bee numbers is attributed to infection with several species of viruses (4) and the wide-spread ectoparasitic mite Varroa destructor (5), which can double as a viral vector. Multiple studies have shown that deformed wing virus (DWV), particularly when associated with high levels of V. destructor infestation, is linked to overwintering losses of colonies and "colony collapse disorder," where the number of adults bees in a particular hive plummets dramatically as a consequence of unexplained factors (3,(6)(7)(8)(9).…”

Spatial evolutionary epidemiology of spreading epidemics

“…In particular, these models highlight the build-up of phenotypic variation between the front and the rear of a spreading epidemic. In accord with these theoretical results, recent field studies report the existence of patterns of phenotypic differentiation between pathogens sampled at the front or at the epicentre of epidemics [19,[23][24][25].…”