Elevated virulence of an emerging viral genotype as a driver of honeybee loss

Abstract

Emerging infectious diseases (EIDs) have contributed significantly to the current biodiversity crisis, leading to widespread epidemics and population loss. Owing to genetic variation in pathogen virulence, a complete understanding of species decline requires the accurate identification and characterization of EIDs. We explore this issue in the Western honeybee, where increasing mortality of populations in the Northern Hemisphere has caused major concern. Specifically, we investigate the importance of genetic identity of the main suspect in mortality, deformed wing virus (DWV), in driving honeybee loss. Using laboratory experiments and a systematic field survey, we demonstrate that an emerging DWV genotype (DWV-B) is more virulent than the established DWV genotype (DWV-A) and is widespread in the landscape. Furthermore, we show in a simple model that colonies infected with DWV-B collapse sooner than colonies infected with DWV-A. We also identify potential for rapid DWV evolution by revealing extensive genome-wide recombination in vivo. The emergence of DWV-B in naive honeybee populations, including via recombination with DWV-A, could be of significant ecological and economic importance. Our findings emphasize that knowledge of pathogen genetic identity and diversity is critical to understanding drivers of species decline.

Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival

“…In particular, DWV-infected bees started to forage at an earlier age and showed reduced lifespans and total activity spans than control bees. Finally, next-gen sequencing demonstrated that the DWV strain we used for inoculation belonged to the type B DWB master variant [52], which has recently been found to be an emergent, more virulent strain of the DWV virus [25] that currently appears to be the most common strain in Britain [25]. The fact that our DWV lysate was prepared from a randomly selected sample of bees with overt DWV infection symptoms suggest that this strain is now also common in Continental Europe.…”

“…The amount of DWV injected was estimated at 1.2 Â 10 4 -4.6 Â 10 5 DWV copies per bee, and was aimed at mimicking infection loads reported for bees with covert infections (1.4 Â 10 3 -2.4 Â 10 9 copies per bee, [51]). Based on Illumina ultrahigh throughput sequencing, the DWV strain used for inoculation was determined to belong to the type B DWV master variant [52], which has recently been found to be an emergent, slightly more virulent strain of the DWV virus [25] that is currently also the most common strain in Britain [25] (for details, see the electronic supplementary material).…”

“…DWV has a near global distribution and is the most widespread of the currently described viruses that infect honeybees, often affecting between 50% and 75% of all honeybee hives [25,26]. In addition, the virus can spill over to other bees [27,28], thereby posing an additional threat.…”

“…Indeed, several recent studies using controlled artificial infection of adult honeybee workers have shown a number of important effects of DWV, including the impairment of sensory responsiveness, associative olfactory learning and memory formation [30] ( possibly linked to replication of the virus in the mushroom bodies and antennal lobes [31]), an accelerated pace of behavioural transition through their age-linked task allocation [32] and reduced lifespans of infected adult honeybees [25]. Furthermore, two studies in which natural variation in infection levels of DWV was combined with experimentally manipulated variation in infection levels with the microsporidian parasite Nosema showed that DWV-infected bees displayed shortened flight distances and flight durations in flight mill experiments [33], but no differences in orientation flight behaviour in a harmonic radar tracking set-up [34], whereas the reverse pattern was seen for Nosema [33,34].…”

Evidence of Varroa-mediated deformed wing virus spillover in Hawaii

“…The known DWV strains (Type A, B, and C), and recombinants thereof, may be linked to differences in DWV virulence in honey bee colonies (Martin et al, 2012;McMahon et al, 2016;Ryabov et al, 2014;Zioni et al, 2011), however, there is no evidence that strains may be specifically linked to wing deformities on bees, rather it appears that viral loads of DWV play a significant role in the expression of this phenotype in honey bees (Brettell et al, 2017). By comparison to the existing work on honey bees, our understanding about DWV transmissibility and its effect on the fitness of non-Apis bees, and other insects, is much more limited.…”