Haemolymph removal by the parasite <i>Varroa destructor</i> can trigger the proliferation of the Deformed Wing Virus in mite infested bees (<i>Apis mellifera</i>), contributing to enhanced pathogen virulence

Annoscia, Desiderato; Brown, Sam P.; Prisco, Gennaro Di; Paoli, Emanuele De; Fabbro, Simone Del; Zanni, Virginia; Galbraith, David A.; Caprio, Emilio; Grozinger, Christina M.; Pennacchio, Francesco; Nazzi, Francesco

doi:10.1101/257667

Cited by 8 publications

(10 citation statements)

References 40 publications

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“…In addition, no significant differences were affirmed between single DWV infection levels (expressed through a Ct value) in colonies of different strength. These results may speak in favour of crucial influence of predisposing factors—pathogens, parasites, poor-quality nutrition, pesticides, and unfavourable climate conditions—on bee vitality ( Stanimirović et al, 2007a ; Simeunovic et al, 2014b ; Abbo et al, 2017 ; Annoscia et al, 2018 ; Glavinic et al, 2017 ; Stevanovic et al, 2016 ). Special emphasis should be put on the negative influence of infestation with V. destructor , a biological and mechanical vector of at least two viruses, DWV and APBV, ( Ryabov et al, 2014 ; Abbo et al, 2017 ) and a possible factor that could contribute Nosema ceranae spreading ( Glavinić et al, 2014 ).…”

Section: Discussionmentioning

confidence: 99%

Honey bee viruses in Serbian colonies of different strength

Ćirković

Stevanović

Glavinić

et al. 2018

PeerJ

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Protection of honey bees is of great economic importance because of their role in pollination. Crucial steps towards this goal are epidemiological surveys of pathogens connected with honey bee losses. In this study deformed wing virus (DWV), chronic bee paralysis virus (CBPV), acute bee paralysis virus (ABPV) and sacbrood virus (SBV) were investigated in colonies of different strength located in five regions of Serbia. The relationship between colony strength and virus occurrence/infection intensity were assessed as well as the genetic relationship between virus sequences from Serbia and worldwide. Real-time RT-PCR analyses detected at least one virus in 87.33% of colonies. Single infection was found in 28.67% colonies (21.33%, 4.00%, 2.67% and 0.67% in cases of DWV, ABPV, SBV and CBPV, respectively). In the majority of colonies (58.66%) more than one virus was found. The most prevalent was DWV (74%), followed by ABPV, SBV and CBPV (49.30%, 24.00% and 6.70%, respectively). Except for DWV, the prevalence of the remaining three viruses significantly varied between the regions. No significant differences were found between colony strength and either (i) the prevalence of DWV, ABPV, SBV, CBPV and their combinations, or (ii) DWV infection levels. The sequences of honey bee viruses obtained from bees in Serbia were 93–99% identical with those deposited in GenBank.

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Section: Discussionmentioning

confidence: 99%

Honey bee viruses in Serbian colonies of different strength

Ćirković

Stevanović

Glavinić

et al. 2018

PeerJ

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“…Several studies suggest that DWV replication in mites and/or mite-mediated virus transmission impacts the diversity of viral genomes at both a geographic scale (i.e., mite induced bottleneck of DWV strains in the Hawaiian Islands [ 86 ]) and at the individual bee level [ 87 , 88 ]. Poor honey bee colony health is associated with high mite infestation coupled with DWV infection [ 83 , 85 , 89 , 90 , 91 , 92 , 93 ] and the seasonal dynamics of mite infestation and DWV abundance are strongly correlated [ 12 , 17 , 54 , 85 , 90 , 93 , 94 , 95 ]. The potential role of parasite-mediated virus transmission is under-explored for other bee species.…”

Section: Introductionmentioning

confidence: 99%

Honey Bee and Bumble Bee Antiviral Defense

McMenamin

Daughenbaugh

Parekh

et al. 2018

Viruses

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Bees are important plant pollinators in both natural and agricultural ecosystems. Managed and wild bees have experienced high average annual colony losses, population declines, and local extinctions in many geographic regions. Multiple factors, including virus infections, impact bee health and longevity. The majority of bee-infecting viruses are positive-sense single-stranded RNA viruses. Bee-infecting viruses often cause asymptomatic infections but may also cause paralysis, deformity or death. The severity of infection is governed by bee host immune responses and influenced by additional biotic and abiotic factors. Herein, we highlight studies that have contributed to the current understanding of antiviral defense in bees, including the Western honey bee (Apis mellifera), the Eastern honey bee (Apis cerana) and bumble bee species (Bombus spp.). Bee antiviral defense mechanisms include RNA interference (RNAi), endocytosis, melanization, encapsulation, autophagy and conserved immune pathways including Jak/STAT (Janus kinase/signal transducer and activator of transcription), JNK (c-Jun N-terminal kinase), MAPK (mitogen-activated protein kinases) and the NF-κB mediated Toll and Imd (immune deficiency) pathways. Studies in Dipteran insects, including the model organism Drosophila melanogaster and pathogen-transmitting mosquitos, provide the framework for understanding bee antiviral defense. However, there are notable differences such as the more prominent role of a non-sequence specific, dsRNA-triggered, virus limiting response in honey bees and bumble bees. This virus-limiting response in bees is akin to pathways in a range of organisms including other invertebrates (i.e., oysters, shrimp and sand flies), as well as the mammalian interferon response. Current and future research aimed at elucidating bee antiviral defense mechanisms may lead to development of strategies that mitigate bee losses, while expanding our understanding of insect antiviral defense and the potential evolutionary relationship between sociality and immune function.

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“…One reason for this persistence is likely the standard protocol of removing hemolymph samples from late-stage larvae and early-stage pupae, a time when large deposits of fat body are present in the hemolymph tissue. If the fat body is not separated carefully from the hemolymph, the molecular/nutritional contents of what is being called hemolymph strongly reflect the molecular/nutritional content of a commingled tissue that is largely fat body (25–27).…”

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confidence: 99%

Varroa destructorfeeds primarily on honey bee fat body tissue and not hemolymph

Ramsey

Ochoa

Bauchan

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

432

322

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SignificanceVarroa destructor causes considerable damage to honey bees and subsequently the field of apiculture through just one process: feeding. For five decades, we have believed that these mites consume hemolymph like a tick consumes blood, and that Varroa cause harm primarily by vectoring viruses. Our work shows that they cause damage more directly. Varroa externally digest and consume fat body tissue rather than blood. These findings explain the failure of some previous attempts at developing effectively targeted treatment strategies for Varroa control. Furthermore, it provides some explanation for the diverse array of debilitating pathologies associated with Varroa that were unexplained by hemolymph removal alone. Our work provides a path forward for the development of novel treatment strategies for Varroa.

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Haemolymph removal by the parasite Varroa destructor can trigger the proliferation of the Deformed Wing Virus in mite infested bees (Apis mellifera), contributing to enhanced pathogen virulence

Cited by 8 publications

References 40 publications

Honey bee viruses in Serbian colonies of different strength

Honey bee viruses in Serbian colonies of different strength

Honey Bee and Bumble Bee Antiviral Defense

Varroa destructorfeeds primarily on honey bee fat body tissue and not hemolymph

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