Global pollinators, like honeybees, are declining in abundance and diversity, which can adversely affect natural ecosystems and agriculture. Therefore, we tested the current hypotheses describing honeybee losses as a multifactorial syndrome, by investigating integrative effects of an infectious organism and an insecticide on honeybee health. We demonstrated that the interaction between the microsporidia Nosema and a neonicotinoid (imidacloprid) significantly weakened honeybees. In the short term, the combination of both agents caused the highest individual mortality rates and energetic stress. By quantifying the strength of immunity at both the individual and social levels, we showed that neither the haemocyte number nor the phenoloxidase activity of individuals was affected by the different treatments. However, the activity of glucose oxidase, enabling bees to sterilize colony and brood food, was significantly decreased only by the combination of both factors compared with control, Nosema or imidacloprid groups, suggesting a synergistic interaction and in the long term a higher susceptibility of the colony to pathogens. This provides the first evidences that interaction between an infectious organism and a chemical can also threaten pollinators, interactions that are widely used to eliminate insect pests in integrative pest management.

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.

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In eusocial insect colonies nestmates cooperate to combat parasites, a trait called social immunity. However, social immunity failed for Western honey bees (Apis mellifera) when the ectoparasitic mite Varroa destructor switched hosts from Eastern honey bees (Apis cerana). This mite has since become the most severe threat to A. mellifera world-wide. Despite this, some isolated A. mellifera populations are known to survive infestations by means of natural selection, largely by supressing mite reproduction, but the underlying mechanisms of this are poorly understood. Here, we show that a cost-effective social immunity mechanism has evolved rapidly and independently in four naturally V. destructor-surviving A. mellifera populations. Worker bees of all four ‘surviving’ populations uncapped/recapped worker brood cells more frequently and targeted mite-infested cells more effectively than workers in local susceptible colonies. Direct experiments confirmed the ability of uncapping/recapping to reduce mite reproductive success without sacrificing nestmates. Our results provide striking evidence that honey bees can overcome exotic parasites with simple qualitative and quantitative adaptive shifts in behaviour. Due to rapid, parallel evolution in four host populations this appears to be a key mechanism explaining survival of mite infested colonies.

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Social immunity forms an essential part of the defence repertoire of social insects. In response to infestation by the parasitic mite Varroa destructor and its associated viruses, honey bees (Apis mellifera L.) have developed a specific behaviour (varroa-sensitive hygiene, or VSH) that helps protect the colony from this parasite. Brood cells heavily infested with mites are uncapped, the brood killed, and the cell contents removed. For this extreme sacrifice to be beneficial to the colony, the targeting of parasitized brood for removal must be accurate and selective. Here we show that varroa-infested brood produce uniquely identifiable cues that could be used by VSH-performing bees to identify with high specificity which brood cells to sacrifice. This selective elimination of mite-infested brood is a disease resistance strategy analogous to programmed cell death, where young bees likely to be highly dysfunctional as adults are sacrificed for the greater good of the colony.

In honey bees, Varroa sensitive hygiene (VSH) behaviour, which involves the detection and removal of brood parasitised by the mite Varroa destructor, can actively participate in the survival of colonies facing Varroa outbreaks. This study investigated the mechanisms of VSH behaviour, by comparing the antennal transcriptomes of bees that do and do not perform VSH behaviour. Results indicate that antennae likely play a key role in the expression of VSH behaviour. Comparisons with the antennal transcriptome of nurse and forager bees suggest that VSH profile is more similar to that of nurse bees than foragers. Enhanced detection of certain odorants in VSH bees may be predicted from transcriptional patterns, as well as a higher metabolism and antennal motor activity. Interestingly, Deformed wing virus/Varroa destructor virus infections were detected in the antennae, with higher level in non-VSH bees; a putative negative impact of viral infection on bees’ ability to display VSH behaviour is proposed. These results bring new perspectives to the understanding of VSH behaviour and the evolution of collective defence by focusing attention on the importance of the peripheral nervous system. In addition, such data might be useful for promoting marker-assisted selection of honey bees that can survive Varroa infestations.

Since its migration from the Asian honey bee (Apis cerana) to the European honey bee (Apis mellifera), the ectoparasitic mite Varroa destructor has emerged as a major issue for beekeeping worldwide. Due to a short history of coevolution, the host–parasite relationship between A. mellifera and V. destructor is unbalanced, with honey bees suffering infestation effects at the individual, colony and population levels. Several control solutions have been developed to tackle the colony and production losses due to Varroa, but the burden caused by the mite in combination with other biotic and abiotic factors continues to increase, weakening the beekeeping industry. In this synthetic review, we highlight the main advances made between 2015 and 2020 on V. destructor biology and its impact on the health of the honey bee, A. mellifera. We also describe the main control solutions that are currently available to fight the mite and place a special focus on new methodological developments, which point to integrated pest management strategies for the control of Varroa in honey bee colonies.