Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera)

Abstract

Deformed wing virus (DWV) is a viral pathogen of the European honeybee (Apis mellifera), associated with clinical symptoms and colony collapse when transmitted by the ectoparasitic mite Varroa destructor. In the absence of V. destructor, DWV infection does not result in visible symptoms, suggesting that mite-independent transmission results in covert infections. True covert infections are a known infection strategy for insect viruses, resulting in long-term persistence of the virus in the population. They are characterized by the absence of disease symptoms in the presence of the virus and by vertical transmission of the virus. To demonstrate vertical transmission and, hence, true covert infections for DWV, a detailed study was performed on the vertical-transmission routes of DWV. In total, 192 unfertilized eggs originating from eight virgin queens, and the same number of fertilized eggs from the same queens after artificial insemination with DWV-negative (three queens) or DWV-positive (five queens) semen, were analysed individually. The F0 queens and drones and F1 drones and workers were also analysed for viral RNA. By in situ hybridization, viral sequences were detected in the ovary of an F0 queen that had laid DWV-positive unfertilized eggs and was inseminated with DWV-positive semen. In conclusion, vertical transmission of DWV from queens and drones to drone and worker offspring through unfertilized and fertilized eggs, respectively, was demonstrated. Viral sequences in fertilized eggs can originate from the queen, as well as from drones via DWV-positive semen.

Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route

“…In the absence of V. destructor, DWV is considered a virus with low virulence that manages to establish vertical transmission routes through both drones and queens (de Miranda & Fries, 2008;Yue et al, 2007). Such vertically transmitted infections are mainly if not exclusively covert, which might present a mechanism for long-term persistence in the honeybee population as has also been described for other insect viruses (Bonsall et al, 2005;Burden et al, 2003;de Miranda & Genersch, 2010;Hails et al, 2008).…”

“…These vertically infected bees also lacked another hallmark of overt DWV infection, the detection of DWV RNA in bees' heads (Yue & Genersch, 2005;Yue et al, 2007). The clinical importance of this characteristic was demonstrated recently.…”

“…Recently, it has been shown that DWV infections can be vertically transmitted through drones and queens and that this transmission route results in covert infections (presence of the virus in the absence of visible symptoms) (de Miranda & Genersch, 2010;de Miranda & Fries, 2008;Yue et al, 2007), which follows the general assumption that vertical transmission selects for less virulent forms of a pathogen (Ewald, 1983;Ewald & De Leo, 2002;Fries & Camazine, 2001). These vertically infected bees also lacked another hallmark of overt DWV infection, the detection of DWV RNA in bees' heads (Yue & Genersch, 2005;Yue et al, 2007).…”

“…DWV normally causes covert infections in honeybees (de Miranda & Fries, 2008;Hails et al, 2008;Yue et al, 2007). Overt DWV infections characterized by the occurrence of visible disease symptoms (deformed wings, bloated and shortened abdomen, and miscolouring) are associated with V. destructor infestation (Ball & Allen, 1988;Bowen-Walker et al, 1999;Martin, 2001;Martin et al, 1998; Santillán-Galicia et al, 2010;Tentcheva et al, 2006;Yue & Genersch, 2005).…”

“…Overt DWV infections characterized by the occurrence of visible disease symptoms (deformed wings, bloated and shortened abdomen, and miscolouring) are associated with V. destructor infestation (Ball & Allen, 1988;Bowen-Walker et al, 1999;Martin, 2001;Martin et al, 1998; Santillán-Galicia et al, 2010;Tentcheva et al, 2006;Yue & Genersch, 2005). However, the exact role of the mite in the pathogenesis of DWV is still not fully understood and a direct causal link between the virus and the symptom 'wing deformity' has not been established yet (de Miranda & Genersch, 2010).Recently, it has been shown that DWV infections can be vertically transmitted through drones and queens and that this transmission route results in covert infections (presence of the virus in the absence of visible symptoms) (de Miranda & Genersch, 2010;de Miranda & Fries, 2008;Yue et al, 2007), which follows the general assumption that vertical transmission selects for less virulent forms of a pathogen (Ewald, 1983;Ewald & De Leo, 2002;Fries & Camazine, 2001). These vertically infected bees also lacked another hallmark of overt DWV infection, the detection of DWV RNA in bees' heads (Yue & Genersch, 2005;Yue et al, 2007).…”