Robert J. Paxton

Background: Over the last two decades, honey bees (Apis mellifera) have suffered high rates of colony losses that have been attributed to a variety of factors, chief among which are viral pathogens, such as deformed wing virus (DWV), whose virulence has increased because of vector-based transmission by the invasive, ectoparasitic varroa mite (Varroa destructor). A shift in the experimental mode of transmission of the black queen cell virus (BQCV) and sacbrood virus (SBV) from fecal/food–oral (direct horizontal) to vector-mediated (indirect horizontal) transmission also results in high virulence and viral titers in pupal and adult honey bees. Agricultural pesticides represent another factor that acts independently or in interaction with pathogens, and they are also thought to cause colony loss. Understanding the molecular mechanisms underlying the higher virulence following a vector-based mode of transmission provides deeper insight into honey bee colony losses, as does determining whether or not host–pathogen interactions are modulated by exposure to pesticides. Methods: Through an experimental design with controlled laboratory, we investigated the effects of the modes of transmission of BQCV and SBV (feeding vs. vector-mediated via injection) alone or in combination with chronic exposure to sublethal and field-realistic concentrations of flupyradifurone (FPF), a novel agricultural insecticide, on honey bee survival and transcription responses by using high-throughput RNA sequencing (RNA-seq) analysis. Results: Co-exposure to viruses via feeding (VF) or injection (VI) and FPF insecticide had no statistically significant interactive effect on their survival compared to, respectively, VF or VI treatments alone. Transcriptomic analysis revealed a distinct difference in the gene expression profiles of bees inoculated with viruses via injection (VI) and exposed to FPF insecticide (VI+FPF). The number of differentially expressed genes (DEGs) at log2 (fold-change) > 2.0 in VI bees (136 genes) or/and VI+FPF insecticide (282 genes) was very high compared to that of VF bees (8 genes) or the VF+FPF insecticide treatment (15 genes). Of these DEGs, the expression in VI and VI+FPF bees of some immune-related genes, such as those for antimicrobial peptides, Ago2, and Dicer, was induced. In short, several genes encoding odorant binding proteins, chemosensory proteins, odor receptors, honey bee venom peptides, and vitellogenin were downregulated in VI and VI+FPF bees. Conclusions: Given the importance of these suppressed genes in honey bees’ innate immunity, eicosanoid biosynthesis, and olfactory associative function, their inhibition because of the change in the mode of infection with BQCV and SBV to vector-mediated transmission (injection into haemocoel) could explain the high virulence observed in these viruses when they were experimentally injected into hosts. These changes may help explain why other viruses, such as DWV, represent such a threat to colony survival when transmitted by varroa mites.

Honey bees are essential for crop and wild plant pollination. However, many countries have reported high annual colony losses caused by multiple possible stressors. Diseases, particularly those caused by viruses, are a major cause of colony losses. However, little is known about the prevalence of honey bee pathogens, particularly virus prevalence, in Egyptian honey bees. To address this shortfall, we determined the prevalence of widespread bee viruses in honey bee colonies in Egypt—whether it is affected by geography, the season, or infestation with Varroa destructor (varroa) mites. Honey bee worker samples were collected from 18 geographical regions across Egypt during two seasons: winter and summer of 2021. Three apiaries were chosen in each region, and a pooled sample of 150 worker bees was collected from five colonies in each apiary then screened by qPCR for 10 viral targets: acute bee paralysis virus (ABPV), black queen cell virus (BQCV), chronic bee paralysis virus (CBPV), deformed wing virus (DWV) genotypes A (DWV-A), B (DWV-B) and D (Egyptian bee virus), Israeli acute paralysis virus (IAPV), Kashmir bee virus (KBV), sacbrood virus (SBV), and slow bee paralysis virus (SBPV). Our results revealed that DWV-A was the most prevalent virus, followed by BQCV and ABPV; the DWV genotype now spreading across the world, DWV-B, was not detected. There was no difference in varroa infestation rates as well as virus prevalence between winter and summer. However, colonies infected with BQCV had a significantly higher varroa count (adjusted p < 0.05) in the winter season, indicating that there is a seasonal association between the intensity of infestation by varroa and the presence of this virus. We provide data on the current virus prevalence in Egypt, which could assist in the protection of Egypt’s beekeeping industry. Moreover, our study aids in the systematic assessment of the global honey bee virome by filling a knowledge gap about the prevalence of honey bee viruses in Egypt.