Shift in virus composition in honeybees (Apis mellifera) following worldwide invasion by the parasitic mite and virus vector Varroa destructor.

Invasive vectors can induce dramatic changes in disease epidemiology. While viral emergence following geographical range expansion of a vector is well known, the influence a vector can have at the level of the host's pathobiome is less well understood. Taking advantage of the formerly heterogeneous spatial distribution of the ectoparasitic mite Varroa destructor that acts as potent virus vector among honeybees Apis mellifera, we investigated the impact of its recent global spread on the viral community of honeybees in a retrospective study of historical samples. We hypothesized that the vector has had an effect on the epidemiology of several bee viruses, potentially altering their transmissibility and/or virulence, and consequently their prevalence, abundance, or both. To test this, we quantified the prevalence and loads of 14 viruses from honeybee samples collected in mite-free and mite-infested populations in four independent geographical regions. The presence of the mite dramatically increased the prevalence and load of deformed wing virus, a cause of unsustainably high colony losses. In addition, several other viruses became more prevalent or were found at higher load in mite-infested areas, including viruses not known to be actively varroa-transmitted, but which may increase opportunistically in varroa-parasitized bees.

Virus infections in honeybee colonies naturally surviving ectoparasitic mite vectors.

Western honeybee populations, Apis mellifera, in Europe have been known to survive infestations of the ectoparasitic mite, Varroa destructor, by means of natural selection. Proposed mechanisms in literature have been focused on the management of this parasite, however literature remains scare on the differences in viral ecology between colonies that have adapted to V. destructor and those that are consistently treated for it. Samples were collected from both a mite-surviving and a sympatric mite-susceptible honeybee population in Norway. The prevalence and abundances of 10 viruses, vectored by the parasite or not, were investigated in adult host workers and pupae as well as in V. destructor mites. Here we show that the mite-vectored Deformed wing virus (DWV-A) is often lower in both abundance and prevalence in the mite-surviving population in tandem with lower phoretic mite infestations compared to the mite susceptible population. However, the non-mite-vectored Black queen cell virus (BQCV), had both a higher abundance and prevalence in the mite-surviving population compared to the susceptible population. The data therefore suggest that general adaptations to virus infections may be unlikely to explain colony survival. Instead, mechanisms suppressing mite reproduction and therefore the impact seem to be more important.

Reproductive success of the parasitic mite (Varroa destructor) is lower in honeybee colonies that target infested cells with recapping.

Cell recapping is a behavioural trait of honeybees (Apis mellifera) where cells with developing pupae are uncapped, inspected, and then recapped, without removing the pupae. The ectoparasitic mite Varroa destructor, unarguably the most destructive pest in apiculture world-wide, invades the cells of developing pupae to feed and reproduce. Honeybees that target mite infested cells with this behaviour may disrupt the reproductive cycle of the mite. Hence, cell recapping has been associated with colony-level declines in mite reproduction. In this study we compared the colony-level efficacy of cell recapping (how often infested cells are recapped) to the average mite fecundity in A. mellifera. Our study populations, known to be adapted to V. destructor, were from Avignon, France, Gotland, Sweden, and Oslo, Norway, and were compared to geographically similar, treated control colonies. The results show that colonies with a higher recapping efficacy also have a lower average mite reproductive success. This pattern was likely driven by the adapted populations as they had the largest proportion of highly-targeted cell recapping. The consistent presence of this trait in mite-resistant and mite-susceptible colonies with varying degrees of expression may make it a good proxy trait for selective breeding on a large scale.

Varroa destructor: A Complex Parasite, Crippling Honey Bees Worldwide.

The parasitic mite, Varroa destructor, has shaken the beekeeping and pollination industries since its spread from its native host, the Asian honey bee (Apis cerana), to the naïve European honey bee (Apis mellifera) used commercially for pollination and honey production around the globe. Varroa is the greatest threat to honey bee health. Worrying observations include increasing acaricide resistance in the varroa population and sinking economic treatment thresholds, suggesting that the mites or their vectored viruses are becoming more virulent. Highly infested weak colonies facilitate mite dispersal and disease transmission to stronger and healthier colonies. Here, we review recent developments in the biology, pathology, and management of varroa, and integrate older knowledge that is less well known.

Reduced Postcapping Period in Honey Bees Surviving Varroa destructor by Means of Natural Selection.

The ectoparasitic mite Varroa destructor is a key factor for colony losses in European honey bee subspecies (Apis mellifera), but it is also known that some host populations have adapted to the mite by means of natural selection. The role of a shorter host brood postcapping period in reducing mite reproductive success has been investigated in other surviving subspecies, however its role in the adaptation of European honey bee populations has not been addressed. Here, we use a common garden approach to compare the length of the worker brood postcapping period in a Norwegian surviving honey bee population with the postcapping period of a local susceptible population. The data show a significantly shorter postcapping period in the surviving population for ~10% of the brood. Since even small differences in postcapping period can significantly reduce mite reproductive success, this mechanism may well contribute to natural colony survival. It appears most likely that several mechanisms acting together produce the full mite-surviving colony phenotype.

Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection.

BACKGROUND: Managed, feral and wild populations of European honey bee subspecies, Apis mellifera, are currently facing severe colony losses globally. There is consensus that the ectoparasitic mite Varroa destructor, that switched hosts from the Eastern honey bee Apis cerana to the Western honey bee A. mellifera, is a key factor driving these losses. For >20 years, breeding efforts have not produced European honey bee colonies that can survive infestations without the need for mite control. However, at least three populations of European honey bees have developed this ability by means of natural selection and have been surviving for >10 years without mite treatments. Reduced mite reproductive success has been suggested as a key factor explaining this natural survival. Here, we report a managed A. mellifera population in Norway, that has been naturally surviving consistent V. destructor infestations for >17 years. METHODS: Surviving colonies and local susceptible controls were evaluated for mite infestation levels, mite reproductive success and two potential mechanisms explaining colony survival: grooming of adult worker bees and Varroa Sensitive Hygiene (VSH): adult workers specifically detecting and removing mite-infested brood. RESULTS: Mite infestation levels were significantly lower in surviving colonies and mite reproductive success was reduced by 30% when compared to the controls. No significant differences were found between surviving and control colonies for either grooming or VSH. DISCUSSION: Our data confirm that reduced mite reproductive success seems to be a key factor for natural survival of infested A. mellifera colonies. However, neither grooming nor VSH seem to explain colony survival. Instead, other behaviors of the adult bees seem to be sufficient to hinder mite reproductive success, because brood for this experiment was taken from susceptible donor colonies only. To mitigate the global impact of V. destructor, we suggest learning more from nature, i.e., identifying the obviously efficient mechanisms favored by natural selection.