Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra's model

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.

Varroa destructor: how does it harm Apis mellifera honey bees and what can be done about it?

“…Both haemocytes and melanin permit the encapsulation of pathogens during infection or wounding, and thus play a role in insect immune response and healing mechanisms [59]. The weakening of honey bee immunity [60,61] may be linked to the finding that mites feed on fat bodies, given that these organs play a major role in immunity [62].…”

Neonicotinoid Clothianidin reduces honey bee immune response and contributes to Varroa mite proliferation

“…However, neonicotinoids are only one of the many stressors impairing honey bee health and survival 5 – 7 . Among these, a preeminent role is played by the mite Varroa destructor , the most important ectoparasite of honey bees, which is a major problem for honey bee colonies in the Northern hemisphere 8 , 9 ; this is largely related to its activity as a vector and activator of DWV 10 , 11 , with which the mite has established a symbiotic association that exacerbates their respective impacts on honey bee health 12 .…”

Hymenoptera associated eukaryotic virome lacks host specificity

“…The worldwide spread of the Varroa destructor parasite facilitated Deformed wing virus (DWV) infections by acting as an active vector (where the virus can replicate in both the vector and the host) (21). Parallel to its role as viral vector, it has been shown that the V. destructor parasite can also influence the immune status of its host (22). Globalization of V. destructor and concomitant DWV infections raised the question what influence DWV plays in colony health.…”