Adaptation to vector‐based transmission in a honeybee virus

Abstract

1. Global pollinator declines as a result of emerging infectious diseases are of major concern. Managed honeybees Apis mellifera are susceptible to numerous parasites and pathogens, many of which appear to be transmissible to sympatric non-Apis taxa. The ectoparasitic mite Varroa destructor is considered to be the most significant threat to honeybees due to its role in vectoring RNA viruses, particularly Deformed wing virus (DWV). Vector transmission of DWV has resulted in the accumulation of high viral loads in honeybees and is often associated with colony death. DWV has two main genotypes, A and B. DWV-A was more prevalent during the initial phase of V. destructor establishment. In recent years, the global prevalence of DWV-B has increased, suggesting that DWV-B is better adapted to vector transmission than DWV-A.2. We aimed to determine the role vector transmission plays in DWV genotype prevalence at a colony level.3. We experimentally increased or decreased the number of V. destructor mites in honeybee colonies, and tracked DWV-A and DWV-B loads over a period of 10 months. 4. Our results show that the two DWV genotypes differ in their response to mite numbers. DWV-A accumulation in honeybees was positively correlated with mite numbers yet DWV-A was largely undetected in the absence of the mite. In contrast, colonies had high loads of DWV-B even when mite numbers were low. DWV-B loads persisted in miticide-treated colonies, indicating that this genotype has a competitive advantage over DWV-A irrespective of mite numbers.

Viral adaptations to vector‐borne transmission can result in complex host–vector–pathogen interactions

“…These results from experimentally manipulated honeybee colonies are in striking accordance with an independent study at the population level: studying honeybee and bumblebee populations in Varroa-free island refugia and in island and mainland sites positive for Varroa, Manley et al (2019) found that the presence of Varroa increased DWV-B prevalence and viral load both in Varroa's honeybee host as well as in wild bumblebees not infested by Varroa, but that DWV-A was virtually absent in the Varroa-free sites (Figure 1). Norton et al (2021) interpret these results as showing that DWV-B's recent increase in Europe and North America is not driven by selective pressure by the vector, which essentially suggests that DWV-B's spread is driven by higher reproductive capacity in honeybees irrespective of vector-borne transmission. Three methodological caveats have to be mentioned here.…”

“…The honeybee Apis mellifera and its recently acquired ectoparasitic mite Varroa destructor present such a rare system, which Norton et al (2021) have used to test whether adaptation to vector-borne transmission can be a driver of the observed evolution of a novel epidemic bee virus variant (Figure 1). V. destructor is native to the East Asian honeybee A. cerana and jumped to the non-native Western honeybee A. mellifera in South-East Asia at the beginning of the 20th century (Anderson & Trueman, 2000).…”

“…To test the effects of vector-borne transmission in the complex super-organism that a free-flying honeybee colony represents, Norton et al (2021) have manipulated the density of the vector by creating high and low mite-level colonies (M+ and M−), using an apiary in the Netherlands. To increase mite density, they elegantly exploited Varroa's life history following a protocol developed by Panziera et al (2017).…”

“…But in the 2000s, a second strain (DWV-B) emerged and has rapidly over-taken DWV-A in many populations in Europe and North America. Norton et al, (2021) have experimentally studied whether the selective advantage of DWV-B over DWV-A is due to adaptation to transmission by the vector at the colony level (Figure 1a). Using a bold experimental design to manipulate the vector density in honeybee colonies, they have shown that only DWV-A depends on high concentrations of the vector to reach detectable viral loads while DWV-B reaches higher viral loads than DWV-A in both scenarios.…”

Critical View on the Importance of Host Defense Strategies on Virus Distribution of Bee Viruses: What Can We Learn from SARS-CoV-2 Variants?

“…However, as V. destructor plays a major role in honeybee viral dynamics, beekeeping practices, such as treatments against V. destructor may affect viral evolution. One of the suggested mechanisms underlying the shift of DWV-A towards DWV-B is that DWV-B may be better adapted to vector-mediated transmission via V. destructor [ 78 , 95 , 96 ]. Furthermore, Norton et al [ 96 ] showed that the prevalence of DWV-A is highly dependent on the mite presence and density.…”