Significance: Honey bees are exposed to a wealth of synergistically interacting stress factors, which may induce colony losses often associated with high infection levels of pathogens. Neonicotinoid insecticides have been reported to enhance the impact of pathogens, but the underlying immune alteration is still obscure. In this study we describe the molecular mechanism through which clothianidin adversely affects the insect immune response and promotes replication of a viral pathogen in honey bees bearing covert infections. Our results shed light on a further level of regulation of the immune response in insects and have implications for bee conservation.

In this paper, we provide easy to use protocols for the collection, identification, diagnosis, rearing, breeding, marking and measurement of infestation rates and fertility of V. destructor.

The health of the honeybee and, indirectly, global crop production are threatened by several biotic and abiotic factors, which play a poorly defined role in the induction of widespread colony losses. Recent descriptive studies suggest that colony losses are often related to the interaction between pathogens and other stress factors, including parasites. Through an integrated analysis of the population and molecular changes associated with the collapse of honeybee colonies infested by the parasitic mite Varroa destructor, we show that this parasite can de-stabilise the within-host dynamics of Deformed wing virus (DWV), transforming a cryptic and vertically transmitted virus into a rapidly replicating killer, which attains lethal levels late in the season. The de-stabilisation of DWV infection is associated with an immunosuppression syndrome, characterized by a strong down-regulation of the transcription factor NF-κB. The centrality of NF-κB in host responses to a range of environmental challenges suggests that this transcription factor can act as a common currency underlying colony collapse that may be triggered by different causes. Our results offer an integrated account for the multifactorial origin of honeybee losses and a new framework for assessing, and possibly mitigating, the impact of environmental challenges on honeybee health. Honeybees are of capital importance for humans since crop production significantly depends upon pollination by these insects. In recent years, widespread collapses of honeybee colonies have been reported throughout the world; unfortunately, despite intense research efforts, the causal agents of such losses are not yet identified, although parasites seem to play a key-role. We combined molecular, field-longitudinal and theoretical approaches to describe the mechanistic basis and dynamical properties of collapse-causing interactions within the multi-parasite community infecting the honeybees. We found that the parasitic mite Varroa destructor can de-stabilise the within-host dynamics of Deformed wing virus (DWV), transforming a cryptic and vertically transmitted virus into a rapidly replicating killer. The de-stabilisation of DWV infection results from a widespread immunosuppression characterized by a strong down-regulation of a member of the gene family NF-κB. This gene family not only plays a central role in insect immunity, but is also involved in intricate cross-talks with a number of physiological and stress response pathways. This suggests that different stress factors may alter the critical balance between viral pathogens and host-defences, promoting intense viral replication in bees harbouring silent infections and subsequent colony collapse. The model we propose can potentially explain the multifactorial origin of bee losses.

Varroa destructor is the most important ectoparasite of Apis mellifera. This review addresses the interactions between the varroa mite, its environment, and the honey bee host, mediated by an impressive number of cues and signals, including semiochemicals regulating crucial steps of the mite's life cycle. Although mechanical stimuli, temperature, and humidity play an important role, chemical communication is the most important channel. Kairomones are used at all stages of the mite's life cycle, and the exploitation of bees' brood pheromones is particularly significant given these compounds function as primer and releaser signals that regulate the social organization of the honey bee colony. V. destructor is a major problem for apiculture, and the search for novel control methods is an essential task for researchers. A detailed study of the ecological interactions of V. destructor is a prerequisite for creating strategies to sustainably manage the parasite.

Significance: The parasitic mite Varroa destructor and the deformed wing virus (DWV) are linked in a mutualistic symbiosis. The mite acts as vector of the viral pathogen, whereas the DWV-induced immunosuppression in honey bees favors mite feeding and reproduction. This functional interaction underpins a rapidly escalating immunosuppression, which can be primed and/or aggravated by a wealth of stress factors that co-trigger colony losses. Our experimental results explain the pivotal role proposed for the Varroa –DWV association in the induction of honey bee colony losses. Here we provide a functional framework for studying the dynamics of this multifactorial syndrome and defining effective strategies to reduce its negative impact on the beekeeping industry.