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The globally distributed ectoparasite  Varroa destructor  is a vector for viral pathogens of the Western honeybee ( Apis mellifera ), in particular the Iflavirus Deformed Wing Virus (DWV). In the absence of  Varroa  low levels DWV occur, generally causing asymptomatic infections. Conversely,  Varroa -infested colonies show markedly elevated virus levels, increased overwintering colony losses, with impairment of pupal development and symptomatic workers. To determine whether changes in the virus population were due  Varroa  amplifying and introducing virulent virus strains and/or suppressing the host immune responses, we exposed  Varroa -naïve larvae to oral and  Varroa -transmitted DWV. We monitored virus levels and diversity in developing pupae and associated  Varroa , the resulting RNAi response and transcriptome changes in the host. Exposed pupae were stratified by  Varroa  association (presence/absence) and virus levels (low/high) into three groups.  Varroa -free pupae all exhibited low levels of a highly diverse DWV population, with those exposed  per os  (group NV) exhibiting changes in the population composition.  Varroa -associated pupae exhibited either low levels of a diverse DWV population (group VL) or high levels of a near-clonal virulent variant of DWV (group VH). These groups and unexposed controls (C) could be also discriminated by principal component analysis of the transcriptome changes observed, which included several genes involved in development and the immune response. All  Varroa  tested contained a diverse replicating DWV population implying the virulent variant present in group VH, and predominating in RNA-seq analysis of temporally and geographically separate  Varroa -infested colonies, was selected upon transmission from  Varroa , a conclusion supported by direct injection of pupae  in vitro  with mixed virus populations. Identification of a virulent variant of DWV, the role of  Varroa  in its transmission and the resulting host transcriptome changes furthers our understanding of this important viral pathogen of honeybees.

A Virulent Strain of Deformed Wing Virus (DWV) of Honeybees (Apis mellifera) Prevails after Varroa destructor-Mediated, or In Vitro, Transmission