Synergistic Parasite-Pathogen Interactions Mediated by Host Immunity Can Drive the Collapse of Honeybee Colonies

Abstract

The health of the honeybee and, indirectly, global crop production are threatened by several biotic and abiotic factors, which play a poorly defined role in the induction of widespread colony losses. Recent descriptive studies suggest that colony losses are often related to the interaction between pathogens and other stress factors, including parasites. Through an integrated analysis of the population and molecular changes associated with the collapse of honeybee colonies infested by the parasitic mite Varroa destructor, we show that this parasite can de-stabilise the within-host dynamics of Deformed wing virus (DWV), transforming a cryptic and vertically transmitted virus into a rapidly replicating killer, which attains lethal levels late in the season. The de-stabilisation of DWV infection is associated with an immunosuppression syndrome, characterized by a strong down-regulation of the transcription factor NF-κB. The centrality of NF-κB in host responses to a range of environmental challenges suggests that this transcription factor can act as a common currency underlying colony collapse that may be triggered by different causes. Our results offer an integrated account for the multifactorial origin of honeybee losses and a new framework for assessing, and possibly mitigating, the impact of environmental challenges on honeybee health.

Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees

“…The analysis of the possible impact on honey bees can be attempted in the framework of the model for bee colony collapse we recently proposed (6). Indeed, these insecticide molecules may act as an additional stress factor which, by negatively affecting the activation of NF-κB, reinforces and exacerbates the negative impact on honey bee immunity of the transcriptional down-regulation of NF-κB observed in bees exposed to the Varroa-DWV association (6) (Fig.…”

“…This indirectly suggests the possible occurrence of reduced immunocompetence in bees challenged by different stress agents. We recently focused on this aspect, showing how the parasitic mite Varroa destructor can destabilize the delicate immune balance, keeping under control the covert infections of the deformed wing virus (DWV) (6). Indeed, intense DWV replication is triggered by the immune challenge induced by mite feeding, which calls upon the cellular pool of a nuclear factor-κB (NF-κB) protein family member (Dorsal-1A) and weakens the antiviral response controlled by the Toll pathway (6).…”

“…We recently focused on this aspect, showing how the parasitic mite Varroa destructor can destabilize the delicate immune balance, keeping under control the covert infections of the deformed wing virus (DWV) (6). Indeed, intense DWV replication is triggered by the immune challenge induced by mite feeding, which calls upon the cellular pool of a nuclear factor-κB (NF-κB) protein family member (Dorsal-1A) and weakens the antiviral response controlled by the Toll pathway (6). This negatively affects different bee functions and may significantly contribute to colony losses (7)(8)(9)(10)(11)(12).…”

Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata)

“…The rarity of DWV in South African or African honeybees, could explain the apparent health of these honeybee populations. Indeed, without the negative effect of this virus on their immune systems (Nazzi et al, 2012;Yang and Cox-Foster, 2005), African honeybees might be in a better position to withstand the negative effects of other pathogens and parasites. However, Africanized honeybees, that are genetically very similar to their African ancestors, (Kraus et al, 2007;Moritz et al, 2005;Schneider et al, 2004) are infected with DWV (Calderón et al, 2003;Ellis and Munn, 2005;Teixeira et al, 2008), but have not experienced large colony losses (Neumann and Carreck, 2010).…”

Negligible uptake and transfer of diet-derived pollen microRNAs in adult honey bees

“…In agreement, oral administration of dsRNA appears to be effective at regulation of gene expression in honey bees. [69][70][71][72][73][74][75][76] In addition, high dose injection of dsRNAs into the hemocoel has been used for delivery and inhibition of target genes in multiple tissues in this species [77][78][79][80][81][82][83][84][85][86] independent of the site of injection, demonstrating that these molecules can be efficiently taken up by disparate tissues once in the open circulatory system. Our results, in conjunction with the previous studies using dsRNA in other insect species, suggest that uptake of longer dsRNAs may be more efficient than shorter miRNAs.…”