Simulated vector transmission differentially influences dynamics of two viral variants of deformed wing virus in honey bees (Apis mellifera)

Abstract

Understanding how vectors alter the interactions between viruses and their hosts is a fundamental question in virology and disease ecology. In honey bees, transmission of deformed wing virus (DWV) by parasitic Varroa mites has been associated with elevated disease and host mortality, and Varroa transmission has been hypothesized to lead to increased viral titres or select for more virulent variants. Here, we mimicked Varroa transmission by serially passaging a mixed population of two DWV variants, A and B, by injection through in vitro reared honey bee pupae and tracking these viral populations through five passages. The DWV-A and DWV-B variant proportions shifted dynamically through passaging, with DWV-B outcompeting DWV-A after one passage, but levels of both variants becoming equivalent by Passage 5. Sequencing analysis revealed a dominant, recombinant DWV-B strain (DWV-A derived 5′ IRES region with the rest of the genome DWV-B), with low nucleotide diversity that decreased through passaging. DWV-A populations had higher nucleotide diversity compared to DWV-B, but this also decreased through passaging. Selection signatures were found across functional regions of the DWV-A and DWV-B genomes, including amino acid mutations in the putative capsid protein region. Simulated vector transmission differentially impacted two closely related viral variants which could influence viral interactions with the host, demonstrating surprising plasticity in vector-host-viral dynamics.

Honey Bee Genetic Stock Determines Deformed Wing Virus Symptom Severity but not Viral Load or Dissemination Following Pupal Exposure

“…Conversely, PBS injection and mite exposure pupal treatment groups induced higher levels of DWV-B but not DWV-A (Figure 2). The elevated levels of DWV-B in the PBS and mite treatment groups are also similar to prior responses seen in adult bees but not necessarily in pupae (Wu et al, 2017;Dubois et al, 2020;Norton et al, 2020;Penn et al, 2021;Ray et al, 2021). The differential responses to viral infection between pupae and adults have been previously documented both in infection levels and in the ability of dsRNA treatments to mitigate infections (Möckel et al, 2011;Desai et al, 2012;Thaduri et al, 2019).…”

Epidemiology of a major honey bee pathogen, deformed wing virus: potential worldwide replacement of genotype A by genotype B

“…Several experimental studies in which honey bee adults and pupae have been inoculated with DWV-A or DWV-B show that DWV-B replicates faster that DWV-A (e.g. McMahon et al, 2016 ; Tehel et al, 2019 ; Norton et al, 2020 ), at least during its first experimental passage through a host pupa ( Ray et al, 2021 ). High titres are generally – though not always – associated with greater pathogen transmission ( Schmid-Hempel, 2011 ), which provides the basis for our initial estimate of μ (the colony-level rate of transmission) to lie at 0.1 and 0.15 for DWV-A and DWV-B, respectively.…”

“…Though a DWV-A/B recombinant with higher virulence than DWV-A was found to predominate in British honey bees in the Warwick-HRI apiary ( Moore et al, 2011 ; Ryabov et al, 2014 ), recombinants have been found to be surprisingly infrequent in more recent analyses of the continental US honey bee population ( Ryabov et al, 2017 ). Furthermore, experimental co-infection of honey bees with DWV-A and a putative DWV-A/B recombinant and passaging through honey bee pupae did not appear to lead to novel recombinants, though the original A/B recombinant was stable over repeated passages ( Ray et al, 2021 ). Finally, Gusachenko et al (2021) found that recombinant DWV did not out-replicate parental variants in laboratory assays (reviewed in Woodford and Evans, 2021 ).…”

“…Viral recombination occurs when a host individual (a host cell) is co-infected, yet our model incorporates interaction between genotypes in co-infected colonies. Co-infection experiments to date have explored recombination in individual host honey bees ( McMahon et al, 2016 ; Ray et al, 2021 ), which are an easier experimental unit of replication than colonies. Though it may seem a reasonable assumption to scale up the impact of viral recombination at the level of the individual to that at the level of the colony, it would be desirable to run colony-level experiments (as opposed to observations) to support this assumption.…”

Transmission of deformed wing virus between Varroa destructor foundresses, mite offspring and infested honey bees

“…Among the major variants, DWV variant B (DWV-B) is more prevalent in Europe, whereas DWV variant A (DWV-A) is widespread in North America [32,[38][39][40][41]. On several occasions, DWV-B has been shown to outcompete DWV-A in laboratory experiments and field surveys [41][42][43][44][45], although the results seem to depend on the methodology followed in the study [46]. The rapid spread of DWV-B in Hawaii following the recent mite invasion also suggests a strong selective advantage of this variant over DWV-A when the parasite is present [28,45].…”