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Abstract
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.
Highlights
Host-pathogen interactions can be broadly divided into asymptomatic or symptomatic infections [1]
We assessed the total levels of Deformed Wing Virus (DWV) viruses in 80 individual pupae by qRT-PCR using a primer pair for a conserved polymerase-coding region, designed to detect all known DWV strains, including DWV, Varroa destructor virus type 1 (VDV-1) and Kakugo virus (KV) (Table S1)
Varroa were reported to vector at least 5 RNA viruses, the picorna-like Iflavirus deformed wing virus (DWV) is of particular interest and importance; deformed wing disease is associated with mite infestation [9] and high levels of DWV exacerbate overwintering colony losses [10]
Summary
Host-pathogen interactions can be broadly divided into asymptomatic or symptomatic infections [1]. In the former, the absence of symptomatic disease is typically due to restricted pathogen replication, which reduces the opportunities for horizontal transmission within its host population. Prolonged survival of the infected host increases the likelihood of vertical transmission of the pathogen [2]. Symptomatic infections are typically characterized by high levels of pathogen replication, with consequent enhanced virulence, thereby maximizing horizontal transmission [1,2,3,4]. The ‘lifestyle choice’ of asymptomatic or symptomatic infection is determined by multiple factors including the duration of host-pathogen co-evolution, host physiology and anti-pathogen responses, routes of transmission and environmental factors. In the case of multi-host pathogens with interspecies transmission, a pathogen’s virulence may increase following introduction of a second host, when the constraint on pathogen virulence in a given host is removed [6]
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