A virulent strain of Deformed Wing Virus (DWV) of Honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission

Eugene V. Ryabov; Graham R. Wood; Jessica M. Fannon; Jonathan D. Moore; James C. Bull; Dave Chandler; Andrew Mead; Nigel Burroughs; David J. Evans

doi:10.1371/journal.ppat.1004230

A virulent strain of Deformed Wing Virus (DWV) of Honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission

Eugene V. Ryabov^*, Graham R. Wood, Jessica M. Fannon, Jonathan D. Moore, James C. Bull, Dave Chandler, Andrew Mead, Nigel Burroughs, David J. Evans

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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-naive 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.

Original language	English
Article number	e1004230
Number of pages	21
Journal	PLoS Pathogens
Volume	10
Issue number	6
DOIs	https://doi.org/10.1371/journal.ppat.1004230
Publication status	Published - 26 Jun 2014

Keywords

Colony collapse disorder
Picorna-like virus
Drosophila hematopoiesis
Antiviral defense
Microarray data

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10.1371/journal.ppat.1004230Licence: CC BY

ryabov2014ppat1004230
Copyright: © 2014 Ryabov et al. 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.
Final published version, 3.14 MBLicence: CC BY

David John Evans
- d.j.evansst-andrews.acuk
- School of Biology - Emeritus Professor
Person: Emeritus Professor

Cite this

@article{f7edc92c3c824992af9b6f46e5de03ef,

title = "A virulent strain of Deformed Wing Virus (DWV) of Honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission",

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-naive 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.",

keywords = "Colony collapse disorder, Picorna-like virus, Drosophila hematopoiesis, Antiviral defense, Microarray data",

author = "Ryabov, {Eugene V.} and Wood, {Graham R.} and Fannon, {Jessica M.} and Moore, {Jonathan D.} and Bull, {James C.} and Dave Chandler and Andrew Mead and Nigel Burroughs and Evans, {David J.}",

note = "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.",

year = "2014",

month = jun,

day = "26",

doi = "10.1371/journal.ppat.1004230",

language = "English",

volume = "10",

journal = "PLoS Pathogens",

issn = "1553-7366",

publisher = "Public Library of Science",

number = "6",

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TY - JOUR

T1 - A virulent strain of Deformed Wing Virus (DWV) of Honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission

AU - Ryabov, Eugene V.

AU - Wood, Graham R.

AU - Fannon, Jessica M.

AU - Moore, Jonathan D.

AU - Bull, James C.

AU - Chandler, Dave

AU - Mead, Andrew

AU - Burroughs, Nigel

AU - Evans, David J.

N1 - 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.

PY - 2014/6/26

Y1 - 2014/6/26

N2 - 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-naive 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.

AB - 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-naive 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.

KW - Colony collapse disorder

KW - Picorna-like virus

KW - Drosophila hematopoiesis

KW - Antiviral defense

KW - Microarray data

U2 - 10.1371/journal.ppat.1004230

DO - 10.1371/journal.ppat.1004230

M3 - Article

SN - 1553-7366

VL - 10

JO - PLoS Pathogens

JF - PLoS Pathogens

IS - 6

M1 - e1004230

ER -

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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