A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

Prisco, Gennaro Di; Annoscia, Desiderato; Margiotta, Marina; Ferrara, Renata; Varricchio, Paola; Zanni, Virginia; Caprio, Emilio; Nazzi, Francesco; Pennacchio, Francesco

doi:10.1073/pnas.1523515113

Cited by 220 publications

(254 citation statements)

References 43 publications

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“…For example, expression of several AMP genes in honey bees was up-regulated following DWV infection of brood [37], while DWV infection, vectored by V . destructor , adversely affected humoral and cellular immune responses in bees [38]. However, Azzami et al [39] reported that the levels of AMPs were not elevated following artificial inoculation with ABPV.…”

Section: Discussionmentioning

confidence: 99%

Effect of Varroa destructor, Wounding and Varroa Homogenate on Gene Expression in Brood and Adult Honey Bees

et al. 2017

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Honey bee (Apis mellifera) gene expression related to immunity for hymenoptaecin (AmHym) and defensin-1 (AmDef-1), longevity for vitellogenin (AmVit2) and stem cell proliferation for poly U binding factor 68 kDa (AmPuf68) was compared following Varroa destructor parasitism, buffer injection and injection of V. destructor compounds in its homogenate. In adults, V. destructor parasitism decreased expression of all four genes, while buffer injection decreased expression of AmHym, AmPuf68 and AmVit2, and homogenate injection decreased expression of AmPuf68 and AmVit2 but increased expression of AmDef-1 relative to their respective controls. The effect of V. destructor parasitism in adults relative to the controls was not significantly different from buffer injection for AmHym and AmVit2 expression, and it was not significantly different from homogenate injection for AmPuf68 and AmVit2. In brood, V. destructor parasitism, buffer injection and homogenate injection decreased AmVit2 expression, whereas AmHym expression was decreased by V. destructor parasitism but increased by buffer and homogenate injection relative to the controls. The effect of varroa parasitism in brood was not significantly different from buffer or homogenate injection for AmPuf68 and AmVit2. Expression levels of the four genes did not correlate with detectable viral levels in either brood or adults. The results of this study indicate that the relative effects of V. destructor parasitism on honey bee gene expression are also shared with other types of stresses. Therefore, some of the effects of V. destructor on honey bees may be mostly due to wounding and injection of foreign compounds into the hemolymph of the bee during parasitism. Although both brood and adults are naturally parasitized by V. destructor, their gene expression responded differently, probably the result of different mechanisms of host responses during development.

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Section: Discussionmentioning

confidence: 99%

Effect of Varroa destructor, Wounding and Varroa Homogenate on Gene Expression in Brood and Adult Honey Bees

et al. 2017

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“…Varroa parasitism and associated viruses affect the honey bee immunity in complex ways (Di Prisco et al, 2016; Kuster et al, 2014) and a long-term suppression of some immune genes had previously been observed (Yang and Cox-Foster, 2005). Varroa parasitism decreases vitellogenin protein titers in the hemolymph of worker honey bees throughout adult life (Amdam et al, 2004a), which contrasts with our results.…”

Section: Discussionmentioning

confidence: 99%

Early life stress affects mortality rate more than social behavior, gene expression or oxidative damage in honey bee workers

Rueppell

Yousefi

Collazo

et al. 2017

Experimental Gerontology

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Early life stressors can affect aging and life expectancy in positive or negative ways. Individuals can adjust their behavior and molecular physiology based on early life experiences but relatively few studies have connected such mechanisms to demographic patterns in social organisms. Sociality buffers individuals from environmental influences and it is unclear how much early life stress affects later life history. Workers of the honey bee (Apis mellifera L.) were exposed to two stressors, Varroa parasitism and paraquat exposure, early in life. Consequences were measured at the molecular, behavioral, and demographic level. While treatments did not significantly affect levels of oxidative damage, expression of select genes, and titers of the common deformed wing virus, most of these measures were affected by age. Some of the age effects, such as declining levels of deformed wing virus and oxidative damage, were opposite to our predictions but may be explained by demographic selection. Further analyses suggested some influences of worker behavior on mortality and indicated weak treatment effects on behavior. The latter effects were inconsistent among the two experiments. However, mortality rate was consistently reduced by Varroa mite stress during development. Thus, mortality was more responsive to early life stress than our other response variables. The lack of treatment effects on these measures may be due to the social organization of honey bees that buffers the individual from the impact of stressful developmental conditions.

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“…The pathogenicity of DWV and the relationship between the virus, the mite, and the honey bee continue to be the focus of much research in honey bee pathology (Di Prisco et al, 2016;Möckel et al, 2010;Ryabov et al, 2014). The known DWV strains (Type A, B, and C), and recombinants thereof, may be linked to differences in DWV virulence in honey bee colonies (Martin et al, 2012;McMahon et al, 2016;Ryabov et al, 2014;Zioni et al, 2011), however, there is no evidence that strains may be specifically linked to wing deformities on bees, rather it appears that viral loads of DWV play a significant role in the expression of this phenotype in honey bees (Brettell et al, 2017).…”

Section: Floral Resources Have Been Identified As a Potential Contactmentioning

confidence: 99%

Evidence of Varroa-mediated deformed wing virus spillover in Hawaii

Santamaria

Villalobos

Brettell

et al. 2018

Journal of Invertebrate Pathology

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Abstract:Varroa destructor, a parasitic mite of honey bees, is also a vector for viral diseases. The mite displays high host specificity and requires access to colonies of Apis spp. to complete its lifecycle. In contrast, the Deformed Wing Virus (DWV), one of the many viruses transmitted by V. destructor, appears to have a much broader host range. Previous studies have detected DWV in a variety of insect groups that are not directly parasitized by the mite. In this study, we take advantage of the discrete distribution of the Varroa mite in the Hawaiian archipelago to compare DWV prevalence on non-Apis flower visitors, and test whether Varroa presence is linked to a "viral spillover". We selected two islands with different viral landscapes: Oahu, where V. destructor has been present since 2007, and Maui, where the mite is absent. We sampled individuals of Apis mellifera, Ceratina smaragdula, Polistes aurifer, and Polistes exclamens, to assess and compare the DWV prevalence in the Hymenoptera community of the two islands. The results indicated that, as expected, honey bee colonies on Oahu have much higher incidence of DWV compared to Maui. Correspondingly, DWV was detected on the Non-Apis Hymenoptera collected from Oahu, but was absent in the species examined on Maui. The study sites selected shared a similar geography, climate, and insect fauna, but differed in the presence of the Varroa mite, suggesting an indirect, but significant, increase on DWV prevalence in the Hymenoptera community on mite-infected islands.

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A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

Cited by 220 publications

References 43 publications

Effect of Varroa destructor, Wounding and Varroa Homogenate on Gene Expression in Brood and Adult Honey Bees

Effect of Varroa destructor, Wounding and Varroa Homogenate on Gene Expression in Brood and Adult Honey Bees

Early life stress affects mortality rate more than social behavior, gene expression or oxidative damage in honey bee workers

Evidence of Varroa-mediated deformed wing virus spillover in Hawaii

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