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.

Author Summary

Honeybees are of capital importance for humans since crop production significantly depends upon pollination by these insects. In recent years, widespread collapses of honeybee colonies have been reported throughout the world; unfortunately, despite intense research efforts, the causal agents of such losses are not yet identified, although parasites seem to play a key-role. We combined molecular, field-longitudinal and theoretical approaches to describe the mechanistic basis and dynamical properties of collapse-causing interactions within the multi-parasite community infecting the honeybees. We found that the parasitic mite Varroa destructor can de-stabilise the within-host dynamics of Deformed wing virus (DWV), transforming a cryptic and vertically transmitted virus into a rapidly replicating killer. The de-stabilisation of DWV infection results from a widespread immunosuppression characterized by a strong down-regulation of a member of the gene family NF-κB. This gene family not only plays a central role in insect immunity, but is also involved in intricate cross-talks with a number of physiological and stress response pathways. This suggests that different stress factors may alter the critical balance between viral pathogens and host-defences, promoting intense viral replication in bees harbouring silent infections and subsequent colony collapse. The model we propose can potentially explain the multifactorial origin of bee losses.