Abstract
The association between the deformed wing virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honeybee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, particularly, the causes of viral proliferation in mite-infested bees. Here, we develop and test a novel hypothesis that mite feeding destabilizes viral immune control through the removal of both virus and immune effectors, triggering uncontrolled viral replication. Our hypothesis is grounded on the predator–prey theory developed by Volterra, which predicts prey proliferation when both predators and preys are constantly removed from the system. Consistent with this hypothesis, we show that the experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. By contrast, we do not find consistent support for alternative proposed mechanisms of viral expansion via mite immune suppression or within-host viral evolution. Our results suggest that haemolymph removal plays an important role in the enhanced pathogen virulence observed in the presence of feeding Varroa mites. Overall, these results provide a new model for the mechanisms driving pathogen–parasite interactions in bees, which ultimately underpin honeybee health decline and colony losses.
Highlights
Efficient pollination is vital for crop production [1] and the honeybee is the prevailing managed insect crop pollinator
Honeybees suffer from a range of adverse factors [2]; in particular, the deformed wing virus (DWV) is implicated in the substantial colony losses reported in many parts of the world [3] and the parasitic mite Varroa destructor plays a key role in virus transmission and replication [4,5]
To clarify the role of the mite in the dynamics of viral infection in honeybees, we evaluated the presence and abundance of DWV in adult bees that were artificially infested with one mite as mature larvae or were not infested with mites as controls; viral presence and titres were evaluated using quantitative real-time polymerase chain reaction with sequence-specific DWV primers
Summary
Efficient pollination is vital for crop production [1] and the honeybee is the prevailing managed insect crop pollinator. On a purely theoretical background, it is possible to hypothesize that the concurrent removal of virus particles and circulating antiviral immune effectors by the blood-feeding mite can generate a dynamic response similar in principle to that observed when both prey and predators are constantly removed from a predator–prey system [19] This apparently counterintuitive circumstance was first explained by Volterra, at the beginning of the last century [19], for describing the 2 unexpected fluctuations of certain fish species in the Adriatic Sea. The proposed model clearly showed that the subtraction of both predators and prey, through fishing, could result in the proliferation of the prey [19]. This type of microecological analysis of host–pathogen interactions has broad implications in the research area of animal parasitology
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