A sting in the spit: widespread cross‐infection of multipleRNAviruses across wild and managed bees

Dino P Mcmahon,Robert J Paxton,Panagiotis Theodorou,Matthias A Fürst,Mark J F Brown,Jesicca Caspar,Sonia Altizer

doi:10.1111/1365-2656.12345

Abstract

Summary Declining populations of bee pollinators are a cause of concern, with major repercussions for biodiversity loss and food security. RNA viruses associated with honeybees represent a potential threat to other insect pollinators, but the extent of this threat is poorly understood.This study aims to attain a detailed understanding of the current and ongoing risk of emerging infectious disease (EID) transmission between managed and wild pollinator species across a wide range of RNA viruses.Within a structured large‐scale national survey across 26 independent sites, we quantify the prevalence and pathogen loads of multiple RNA viruses in co‐occurring managed honeybee (Apis mellifera) and wild bumblebee (Bombus spp.) populations. We then construct models that compare virus prevalence between wild and managed pollinators.Multiple RNA viruses associated with honeybees are widespread in sympatric wild bumblebee populations. Virus prevalence in honeybees is a significant predictor of virus prevalence in bumblebees, but we remain cautious in speculating over the principle direction of pathogen transmission. We demonstrate species‐specific differences in prevalence, indicating significant variation in disease susceptibility or tolerance. Pathogen loads within individual bumblebees may be high and in the case of at least one RNA virus, prevalence is higher in wild bumblebees than in managed honeybee populations.Our findings indicate widespread transmission of RNA viruses between managed and wild bee pollinators, pointing to an interconnected network of potential disease pressures within and among pollinator species. In the context of the biodiversity crisis, our study emphasizes the importance of targeting a wide range of pathogens and defining host associations when considering potential drivers of population decline.

Highlights

The ongoing biodiversity crisis threatens human health and global food security (Cardinale et al 2012)
The mite has risen to prominence due to its ability to act as a vector of several RNA viruses that previously persisted relatively benignly in honeybee colonies, most notably deformed wing virus (DWV), and viruses belonging to the acute bee paralysis virus (ABPV) complex (Genersch & Aubert 2010) and slow bee paralysis virus (SBPV) (Carreck, Ball & Martin 2010; Santillan-Galicia et al 2014)
ABPV/IAPV/KBV are thought to be distinct viruses, we refer to the ABPV complex as ‘ABPV’ from hereon, due to the inability to detect either IAPV or KBV in any sample

Summary

Introduction

The ongoing biodiversity crisis threatens human health and global food security (Cardinale et al 2012). Infectious diseases may emerge through association with a host species (a ‘reservoir’) in which pathogens have become established, or where disease epidemiology may have recently changed due to perturbation (e.g. through arrival of a novel disease, or disease vector). The switching of pathogens between host species is a major cause of epidemics in humans and other vertebrate hosts (Woolhouse, Haydon & Antia 2005), and EIDs have potentially profound impacts on invertebrates providing important ecosystem services, which secure food production. Bees provide an essential ecosystem service in the form of crop pollination (Klein et al 2007), but they are under pressure globally (Biesmeijer et al 2006; Goulson, Lye & Darvill 2008; Brown & Paxton 2009; Williams & Osborne 2009; Potts et al 2010; Vanbergen et al 2013). In the case of DWV, the arrival of V. destructor has been directly linked to increased prevalence and virus loads in honeybees (Martin et al 2012)

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