Deformed wing virus
Introduction
Wing deformities in honeybees (Apis mellifera L.) (Fig. 1) have long been associated with a virus, appropriately named deformed wing virus (DWV), transmitted by the ectoparasitic mite Varroa destructor (V. destructor). These deformities are symptomatic of the final stages of colony collapse due to uncontrolled mite infestation and as a result DWV is now one of the main viruses associated with the collapse of honeybee colonies due to infestation with V. destructor (Ball, 1983, Ball and Allen, 1988, Bowen-Walker et al., 1999, Nordström et al., 1999, Ribière et al., 2008, Sumpter and Martin, 2004, Tentcheva et al., 2004b). Examination of the first samples of deformed bees in the early 1980s revealed very high titers of a rather unstable icosahedral virus with a single strand RNA genome (Bailey and Ball, 1991). Subsequent studies using a variety of techniques confirmed a nearly 100% association of the wing deformities with highly elevated titers of the virus and reduced titers in phenotypically normal bees from the same colonies (Bowen-Walker et al., 1999, Chen et al., 2005a, Nordström, 2000, Nordström, 2003, Tentcheva et al., 2006, Tentcheva et al., 2004a, Yue and Genersch, 2005). Nevertheless, a direct causal link between the virus and the symptoms has been difficult to establish, mostly due to the difficulty of excluding other pathogens from contributing to the symptoms.
In the absence of V. destructor DWV normally persists at low levels within the bee colony with no detrimental effect, and can be found in all life stages, from egg to adult bee as well as in the glandular secretions used to feed larvae and the queen (Chen et al., 2005a, Chen et al., 2006b, Yue and Genersch, 2005). DWV is transmitted between bees by both horizontal (faecal–cannibal–oral) and vertical (parent–offspring) transmission (Chen et al., 2006b, Chen et al., 2005b, Yue and Genersch, 2005, Yue et al., 2006, Yue et al., 2007, de Miranda and Fries, 2008).
In this review, we will briefly describe the history and distribution of DWV. Second, we will discuss the genetics of DWV and its close relatives, Varroa destructor virus-1 (VaDV-1) (Ongus et al., 2004) and Kakugo virus (KV) (Fujiyuki et al., 2004) with special emphasis on the quasispecies concept (Eigen, 1993, Eigen, 1996) which may help to explain the sequence diversity found within the DWV/VaDV-1/KV group. Third, we will introduce the terms covert infection and overt infection and discuss how these terms can be applied to better understand the pathology of DWV. Finally, we will describe the transmission routes of DWV and the distinction between horizontal and vertical transmission, which is important for moulding pathogen virulence both at the individual bee level and at the colony level (Chen et al., 2006a, Fries and Camazine, 2001).
Section snippets
History and distribution of DWV
The history, distribution and pathology of DWV have been reviewed in great detail recently (Ribière et al., 2008). DWV was first known as Egypt bee virus (EBV), which was isolated from asymptomatic adult bees collected in Egypt in 1977 (Bailey et al., 1979). Subsequently, a virus isolated from deformed adult bees collected in Japan in 1982 was found to be distantly related to EBV by serology, and briefly named the Japanese isolate of EBV, before being renamed deformed wing virus after the
Genetics of DWV
DWV produces a 30 nm icosahedral particle consisting of a single, positive strand RNA genome and three major structural proteins (Bailey and Ball, 1991, Lanzi et al., 2006, Ongus et al., 2004), characteristics that are common to many picorna-like insect viruses (Moore and Eley, 1991). The genome organization of DWV and VaDV-1 (Fig. 2) is typical of the iflaviruses, a genus of the recently formalized picorna-like family Iflaviridae, and consists of a single open reading frame (ORF) flanked by a
Pathology of DWV
Honeybee pathologists use various terms to describe the outcome of viral infections in honeybees. We surveyed the literature and found consensus that most honeybee viruses normally cause infections without any clinical symptoms. However, when describing this type of infection various terms such as asymptomatic infection, inapparent infection (Bailey and Woods, 1974, Sumpter and Martin, 2004), persistent latent infection (Chen et al., 2005a), persistent benign infection (Martin, 2001), and
Transmission and virulence
The topic of transmission and virulence of DWV cannot be addressed without first defining the term virulence and the related term pathogenicity since especially in invertebrate pathology different definitions for these terms exist (Shapiro-Ilan et al., 2005, Thomas and Elkinton, 2004). For a given host and pathogen, pathogenicity is absolute whereas virulence is variable, e.g., due to strain or environmental effects. Pathogenicity is a qualitative term. An organism is either pathogenic to a
Conflicts of interest
There are no conflicts of interest to be declared.
Acknowledgments
Work presented in this review was supported by a European Commission STREP Grant (FOOD-CT-2006-022568) and Jordbruksverket (JdM) and by the EU (according to regulation 797/2004) as well as by grants from the Ministries of Agriculture of Brandenburg, Sachsen, and Thüringen, and the Senate of Berlin, Germany (EG).
References (174)
- et al.
Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency
Curr. Biol.
(2008) Viruses attacking the honeybee
Adv. Virus Res.
(1976)Divergent picornavirus IRES elements
Virus Res.
(2009)- et al.
The error threshold
Virus Res.
(2005) - et al.
The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud
J. Invertebr. Pathol
(1999) - et al.
Minority memory genomes can influence the evolution of HIV-1 quasispecies in vivo
Gene
(2006) - et al.
Memory in retroviral quasispecies: experimental evidence and theoretical model for human immunodeficiency virus
J. Mol. Biol.
(2003) - et al.
Detection of chronic bee paralysis virus (CBPV) genome and its replicative RNA form in various hosts and possible ways of spread
Virus Res.
(2008) - et al.
Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera
J. Invertebr. Pathol.
(2006) - et al.
Detection of multiple viruses in queens of the honey bee Apis mellifera L
J. Invertebr. Pathol.
(2005)
Virulence evolution and the timing of disease life-history events
Trends Ecol. Evol.
The acute bee paralysis virus – Kashmir bee virus – Israeli acute paralysis virus complex
J. Invertebr. Pathol.
Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.)
J. Invertebr. Pathol.
Akt and foxo dysregulation contribute to infection-induced wasting in Drosophila
Curr. Biol.
Challenging the trade-off model for the evolution of virulence: is virulence management feasible?
Trends Microbiol.
Towards an understanding of the molecular basis of herpes simplex virus latency
Virus Res.
On the nature of virus quasispecies
Trends Microbiol.
Relevance of RNA structure for the activity of picornavirus IRES elements
Virus Res.
Prevalence of pathogenic bee viruses in Hungarian apiaries: situation before joining the European Union
J. Invertebr. Pathol.
Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities
J. Invertebr. Pathol.
Foot-and-mouth disease virus leader proteinase: involvement of C-terminal residues in self-processing and cleavage of eIF4GI
J. Biol. Chem.
Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases: a distinct protein superfamily with a common structural fold
FEBS Lett.
Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha- and coronaviruses
FEBS Lett.
The roles of microRNAs in mammalian virus infection
Biochim. Biophys. Acta
Genetics, pathogenesis and evolution of picornaviruses
Divergent IRES elements in invertebrates
Virus Res.
Vertical transmission of nucleopolyhedrosis virus in insects
J. Invertebr. Pathol.
Virulence and transmissibility of pathogens: what is the relationship?
Trends Microbiol.
The global stock of domesticated honey bees is growing slower than agricultural demand for pollination
Curr. Biol.
Varroa jacobsoni: a prospective pest of honeybees in many parts of the world
Bee World
The incidence and world distribution of honey bee viruses
Bee World
Reduced pollen collection by honey-bee (Hymenoptera, Apidae) colonies infected with Nosema apis and sacbrood virus
J. Econ. Entomol.
The purification and properties of chronic bee-paralysis virus
J. Gen. Virol.
Honey Bee Pathology
Egypt bee virus and Australian isolates of Kashmir bee virus
J. Gen. Virol.
Effects of sacbrood virus on adult honey bees
Ann. Appl. Biol.
Three previously undescribed viruses from the honey bee
J. Gen. Virol.
The association of Varroa jacobsoni with virus diseases of honey bees
Exp. Appl. Acarol.
The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni
Ann. Appl. Biol.
Viruses
Occurence of six honeybee viruses in diseased Austrian apiaries
Appl. Environ. Microbiol.
Phylogenetic analysis of deformed wing virus genotypes from diverse geographic origins indicates recent global distribution of the virus
Appl. Environ. Microbiol.
Role for the P4 amino acid residue in substrate utilization by the poliovirus 3CD proteinase
J. Virol.
Vertical transmission of sublethal granulovirus infection in the Indian meal moth, Plodia interpunctuella
Mol. Ecol.
Covert infections as a mechanism for long-term persistence of baculoviruses
Ecol. Lett.
Molecular characterisation of honey bee viruses
Host pathogen interactions: redefining the basic concepts of virulence and pathogenicity
Infect. Immun.
Different evolutionary patterns are found within human immunodeficiency virus type 1-infected patients
J. Gen. Virol.
Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.)
Appl. Environ. Microbiol.
Cited by (403)
Varroa destructor exacerbates the negative effect of cold contributing to honey bee mortality
2023, Journal of Insect PhysiologyReplicative DWV type A in Bombus terrestris in Pantelleria island (Sicily, Italy)
2023, Journal of Asia-Pacific EntomologyWild lime psyllid Leuronota fagarae Burckhardt (Hemiptera: Psylloidea) picorna-like virus full genome annotation and classification
2023, Journal of Invertebrate PathologyMediating a host cell signaling pathway linked to overwinter mortality offers a promising therapeutic approach for improving bee health
2023, Journal of Advanced ResearchHost brood traits, independent of adult behaviours, reduce Varroa destructor mite reproduction in resistant honeybee populations
2023, International Journal for ParasitologyTransmission modes and efficiency of iflavirus and cripavirus in Queensland fruit fly, Bactrocera tryoni
2023, Journal of Invertebrate Pathology