Viral transmission in honey bees and native bees, supported by a global black queen cell virus phylogeny

Abstract

Summary In recent decades, we have realized that honey bee viruses are not, in fact, exclusive to honey bees. The potential impact of Apis‐affiliated viruses on native pollinators is prompting concern. Our research addresses the issue of virus crossover between honey bees and native bees foraging in the same localities. We measured the presence of black queen cell virus (BQCV), deformed wing virus (DWV) and sacbrood virus (SBV) in managed Apis mellifera (honey bees) and native Andrena spp. (subgenus Melandrena) bee populations in five commercial orchards. We identified viral presence across sites and bees and related these data to measures of bee community diversity. All viruses were found in both managed and native bees, and BQCV was the most common virus in each. To establish evidence for viral crossover between taxa, we undertook an additional examination of BQCV where 74 samples were sequenced and placed in a global phylogenic framework of hundreds of BQCV strains. We demonstrate pathogen sharing across managed honey bees and distantly related wild bees. This phylogenetic analysis contributes to growing evidence for host switching and places local incidence patterns in a worldwide context, revealing multispecies viral transmission.

Genetic Strain Diversity of Multi-Host RNA Viruses that Infect a Wide Range of Pollinators and Associates is Shaped by Geographic Origins

“…To understand the current epidemic of bee viruses, it is key to determine the role of the host species and geographic distribution [12,65]. By placing the sequences generated in this study within a global phylogeny, we found that both KBV and DWV showed strong grouping by geographic regions.…”

“…Viral infections have been extensively studied in the European honey bee (Apis mellifera) because a number of RNA viruses that are circulating within bee populations have been associated with reduced health and reports of colony collapses [8,9]. Increasing evidence suggests that many of these pathogens are not specific to honey bees and instead are shared between many pollinator species and associated arthropods, including bumble bees and other wild bees [10][11][12]; bee predators, such as wasps [10,11]; and scavenging insects, such as ants, cockroaches, and beetles [10,[13][14][15]. Many of these host species have been found cohabiting in bee hives [13,15,16] or share floral resources with honey bees [17][18][19][20].…”

“…Thus far, transmission routes between species are poorly understood; flowers have been suggested to represent "disease transmission hubs" [27], allowing for transmission without direct interactions among species. Closely related viral strains in several pollinators [10] and clustering of virus strains within geographic regions [12,13,20] indicate that ongoing inter-species virus transmission occurs. In order to improve pollinator conservation, multi-host viruses need to be studied further and outside the Apis genus [6].…”

The detection of honey bee (Apis mellifera)-associated viruses in ants

“…Six of the most commonly occurring honey bee-associated viruses include Deformed wing virus (DWV), Black queen cell virus (BQCV), Israeli acute paralysis virus (IAPV), Acute bee paralysis virus (ABPV), Kashmir bee virus (KBV), and Sacbrood virus (SBV) 2 . Although the above listed are commonly referred to as honey bee viruses, previous research has detected these viruses in a number of other arthropods including the ectoparasitic mite Varroa destructor 3,4 , other insect pollinators such as hoverflies, bumblebees, and solitary bees [5][6][7][8][9][10][11][12][13][14][15][16][17][18][19] , and other Hymenopteran insects including some wasps and ants 15,20-28 . Both direct and indirect interactions between honey bees and some of these arthropods (e.g., foraging at the same floral resource, parasitism, and predation) have been proposed as possible routes in which interspecies transmission of honey bee-associated viruses can occur 29-32 .In the southern United States, ants are ubiquitous within apiaries and are common pests of managed honey bees 33 .…”

Host density drives viral, but not trypanosome, transmission in a key pollinator

“…Our experiment examined within-species transmission, but, as noted above, in the wild bumblebees live in complex multispecies assemblages of floral visitors. An increasing number of studies suggest that between-species transmission, in particular from managed honeybees, may be driving emergent diseases in wild pollinators [30,33,34,45,56,57,[63][64][65]. As such, the next obvious step would be to conduct controlled semi-field trials to understand transmission dynamics of viruses between honeybees and bumblebees [34].…”