Deformed wing virus

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Abstract

Deformed wing virus (DWV; Iflaviridae) is one of many viruses infecting honeybees and one of the most heavily investigated due to its close association with honeybee colony collapse induced by Varroa destructor. In the absence of V. destructor DWV infection does not result in visible symptoms or any apparent negative impact on host fitness. However, for reasons that are still not fully understood, the transmission of DWV by V. destructor to the developing pupae causes clinical symptoms, including pupal death and adult bees emerging with deformed wings, a bloated, shortened abdomen and discolouration. These bees are not viable and die soon after emergence. In this review we will summarize the historical and recent data on DWV and its relatives, covering the genetics, pathobiology, and transmission of this important viral honeybee pathogen, and discuss these within the wider theoretical concepts relating to the genetic variability and population structure of RNA viruses, the evolution of virulence and the development of disease symptoms.

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).

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