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

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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.

          Author Summary

          Honeybees are the most important managed pollinating insect, contributing billions of dollars to annual global agricultural production. Over the last century a parasitic mite, Varroa, has spread worldwide, with significant impacts on honeybee colony health as a consequence of its transmission of a cocktail of viruses while feeding on honeybee ‘blood’. The most important virus for colony health is deformed wing virus (DWV), high levels of which cause developmental deformities and premature ageing resulting in high overwintering colony losses. In experiments on individual Varroa-exposed pupae we demonstrate that a single type of virulent DWV is amplified 1,000–10,000 times in the recipient pupae, despite the mite containing a high diversity of replicating DWV strains. We could recapitulate this by direct injection of pupae with mixed virus populations, showing the virulent strain is advantaged by the route of transmission. In parallel, we detected changes in the immune response and developmental gene expression of the honeybee and propose that these contribute to the characteristic pathogenesis of DWV. Identification of a virulent strain of DWV has implications for therapeutic or prophylactic interventions to improve honeybee colony health, as well as contributing to our understanding of the biology of this important honeybee viral pathogen.

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          Most cited references42

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          Gene Ontology: tool for the unification of biology

          Genomic sequencing has made it clear that a large fraction of the genes specifying the core biological functions are shared by all eukaryotes. Knowledge of the biological role of such shared proteins in one organism can often be transferred to other organisms. The goal of the Gene Ontology Consortium is to produce a dynamic, controlled vocabulary that can be applied to all eukaryotes even as knowledge of gene and protein roles in cells is accumulating and changing. To this end, three independent ontologies accessible on the World-Wide Web (http://www.geneontology.org) are being constructed: biological process, molecular function and cellular component.
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            Immune pathways and defence mechanisms in honey bees Apis mellifera

            Social insects are able to mount both group-level and individual defences against pathogens. Here we focus on individual defences, by presenting a genome-wide analysis of immunity in a social insect, the honey bee Apis mellifera. We present honey bee models for each of four signalling pathways associated with immunity, identifying plausible orthologues for nearly all predicted pathway members. When compared to the sequenced Drosophila and Anopheles genomes, honey bees possess roughly one-third as many genes in 17 gene families implicated in insect immunity. We suggest that an implied reduction in immune flexibility in bees reflects either the strength of social barriers to disease, or a tendency for bees to be attacked by a limited set of highly coevolved pathogens.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Pathog
                PLoS Pathog
                plos
                plospath
                PLoS Pathogens
                Public Library of Science (San Francisco, USA )
                1553-7366
                1553-7374
                June 2014
                26 June 2014
                : 10
                : 6
                : e1004230
                Affiliations
                [1 ]School of Life Sciences, University of Warwick, Coventry, United Kingdom
                [2 ]Warwick Systems Biology Centre, University of Warwick, Coventry, United Kingdom
                [3 ]Life Sciences & Warwick Crop Centre, University of Warwick, Wellesbourne, Warwickshire, United Kingdom
                Stanford University, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: EVR DJE DC JCB NB AM. Performed the experiments: EVR JMF GRW. Analyzed the data: EVR GRW JDM JCB NB DJE. Contributed reagents/materials/analysis tools: EVR DJE GRW JDM. Wrote the paper: EVR DJE GRW NB DC.

                [¤a]

                Current address: Department of Biosciences, Wallace Building, Swansea University, Singleton Park, Swansea, United Kingdom

                [¤b]

                Current address: Department of Computational and Systems Biology, Rothamsted Research, Harpenden, Hertfordshire, United Kingdom

                Article
                PPATHOGENS-D-14-00760
                10.1371/journal.ppat.1004230
                4072795
                24968198
                7e360edd-a644-4779-a1e5-5db762b13597
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 28 March 2014
                : 30 April 2014
                Page count
                Pages: 21
                Funding
                This work was supported by the Biotechnology and Biological Sciences Research Council, the Department for Environment, Food and Rural Affairs, the Natural Environment Research Council, the Scottish Government and the Wellcome Trust, under the Insect Pollinators Initiative (grant #BBI0008281, http://www.bbsrc.ac.uk/pollinators) and by University of Warwick HEIF5 Proof of Concept funding to DJE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and life sciences
                Computational Biology
                Genome Analysis
                Transcriptome Analysis
                Genome Evolution
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Evolutionary Biology
                Molecular Evolution
                Molecular biology
                Molecular biology techniques
                Molecular biology assays and analysis techniques
                Nucleic acid analysis
                RNA analysis
                Phylogenetic Analysis
                Sequencing techniques
                Sequence analysis
                RNA sequence analysis
                High Throughput Sequencing
                Nucleic Acid Sequencing
                Parasitology
                Parasite Evolution
                Veterinary Parasitology
                Species Interactions
                Veterinary Science
                Veterinary Diseases
                Epizootics
                Veterinary Virology
                Veterinary Pathology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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