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Viruses transmitted by arthropods pose a huge risk to human health. Wolbachia is an endosymbiotic bacterium that infects various arthropods and can block the viral replication cycle of several medically important viruses. As such, it has been successfully implemented in vector control strategies against mosquito-borne diseases, including Dengue virus. Whilst the mechanisms behind Wolbachia -mediated viral blocking are not fully characterised, it was recently shown that viruses grown in the presence of Wolbachia in some Dipteran cell cultures are less infectious than those grown in the absence of Wolbachia . Here, we investigate the breadth of this mechanism by determining if Wolbachia reduces infectivity in a different system at a different scale. To do this, we looked at Wolbachia’s impact on insect viruses from two diverse virus families within the whole organism Drosophila melanogaster . Drosophila C virus (DCV; Family Dicistroviridae) and Flock House virus (FHV; Famliy Nodaviridae ) were grown in adult D. melanogaster flies with and without Wolbachia strain w MelPop. Measures of the physical characteristics, infectivity, pathogenicity, and replicative properties of progeny virus particles did not identify any impact of Wolbachia on either DCV or FHV. Therefore, there was no evidence that changes in infectivity contribute to Wolbachia- mediated viral blocking in this system. Overall, this is consistent with growing evidence that the mechanisms behind Wolbachia viral blocking are dependent on the unique tripartite interactions occurring between the host, the Wolbachia strain, and the infecting virus.

RNA viruses, once considered specific to honey bees, are suspected of spilling over from managed bees into wild pollinators; however, transmission routes are largely unknown. A widely accepted yet untested hypothesis states that flowers serve as bridges in the transmission of viruses between bees. Here, using a series of controlled experiments with captive bee colonies, we examined the role of flowers in bee virus transmission. We first examined if honey bees deposit viruses on flowers and whether bumble bees become infected after visiting contaminated flowers. We then examined whether plant species differ in their propensity to harbor viruses and if bee visitation rates increase the likelihood of virus deposition on flowers. Our experiment demonstrated, for the first time, that honey bees deposit viruses on flowers. However, the two viruses we examined, black queen cell virus (BQCV) and deformed wing virus (DWV), were not equally distributed across plant species, suggesting that differences in floral traits, virus ecology and/or foraging behavior may mediate the likelihood of deposition. Bumble bees did not become infected after visiting flowers previously visited by honey bees suggesting that transmission via flowers may be a rare occurrence and contingent on multiplicative factors and probabilities such as infectivity of virus strain across bee species, immunocompetence, virus virulence, virus load, and the probability a bumble bee will contact a virus particle on a flower. Our study is among the first to experimentally examine the role of flowers in bee virus transmission and uncovers promising avenues for future research.

Honey bees (Apis mellifera) can be infected by many viruses, some of which pose a major threat to their health and well-being. A critical step in the dynamics of a viral infection is its mode of transmission. Here, we compared for the first time the effect of mode of horizontal transmission of Black queen cell virus (BQCV), a ubiquitous and highly prevalent virus of A. mellifera, on viral virulence in individual adult honey bees. Hosts were exposed to BQCV either by feeding (representing direct transmission) or by injection into hemolymph (analogous to indirect or vector-mediated transmission) through a controlled laboratory experimental design. Mortality, viral titer and expression of three key innate immune-related genes were then quantified. Injecting BQCV directly into hemolymph in the hemocoel resulted in far higher mortality as well as increased viral titer and significant change in the expression of key components of the RNAi pathway compared to feeding honey bees BQCV. Our results support the hypothesis that mode of horizontal transmission determines BQCV virulence in honey bees. BQCV is currently considered a benign viral pathogen of adult honey bees, possibly because its mode of horizontal transmission is primarily direct, per os. We anticipate adverse health effects on honey bees if BQCV transmission becomes vector-mediated.

The arrival of the ectoparasitic mite Varroa destructor on the western honeybee Apis mellifera saw a change in the diversity and prevalence of honeybee RNA viruses. One virus in particular, deformed wing virus (DWV) has become closely associated with V. destructor, leading many to conclude that V. destructor has affected viral virulence by changing the mode of transmission. While DWV is normally transmitted via feeding and faeces, V. destructor transmits viruses by direct injection. This change could have resulted in higher viral prevalence causing increased damage to the bees. Here we test the effect of a change in the mode of transmission on the composition and levels of honeybee RNA viruses in the absence of V. destructor. We find a rapid increase in levels of two viruses, sacbrood virus (SBV) and black queen cell virus (BQCV) after direct injection of viral extracts into honeybee pupae. In pupae injected with high levels of DWV extracted from symptomatic adult bees, DWV levels rapidly decline in the presence of SBV and BQCV. Further, we observe high mortality in honeybee pupae when injected with SBV and BQCV, whereas injecting pupae with high levels of DWV results in near 100% survival. Our results suggest a different explanation for the observed association between V. destructor and DWV. Instead of V. destructor causing an increase in DWV virulence, we hypothesize that direct virus inoculation, such as that mediated by a vector, quickly eliminates the most virulent honeybee viruses resulting in an association with less virulent viruses such as DWV.

Viruses from the family Iflaviridae are insect pathogens. Many of them, including slow bee paralysis virus (SBPV), cause lethal diseases in honeybees and bumblebees, resulting in agricultural losses. Iflaviruses have nonenveloped icosahedral virions containing single-stranded RNA genomes. However, their genome release mechanism is unknown. Here, we show that low pH promotes SBPV genome release, indicating that the virus may use endosomes to enter host cells. We used cryo-EM to study a heterogeneous population of SBPV virions at pH 5.5. We determined the structures of SBPV particles before and after genome release to resolutions of 3.3 and 3.4 Å, respectively. The capsids of SBPV virions in low pH are not expanded. Thus, SBPV does not appear to form “altered” particles with pores in their capsids before genome release, as is the case in many related picornaviruses. The egress of the genome from SBPV virions is associated with a loss of interpentamer contacts mediated by N-terminal arms of VP2 capsid proteins, which result in the expansion of the capsid. Pores that are 7 Å in diameter form around icosahedral threefold symmetry axes. We speculate that they serve as channels for the genome release. Our findings provide an atomic-level characterization of the genome release mechanism of iflaviruses.

Social insect reproductives exhibit exceptional longevity instead of the classic trade-off between somatic maintenance and reproduction. Even normally sterile workers experience a significant increase in life expectancy when they assume a reproductive role. The mechanisms that enable the positive relation between the antagonistic demands of reproduction and somatic maintenance are unclear. To isolate the effect of reproductive activation, honeybee workers were induced to activate their ovaries. These reproductively activated workers were compared to controls for survival and gene expression patterns after exposure to Israeli Acute Paralysis Virus or the oxidative stressor paraquat. Reproductive activation increased survival, indicating better immunity and oxidative stress resistance. After qPCR analysis confirmed our experimental treatments at the physiological level, whole transcriptome analysis revealed that paraquat treatment significantly changed the expression of 1277 genes in the control workers but only two genes in reproductively activated workers, indicating that reproductive activation preemptively protects against oxidative stress. Significant overlap between genes that were upregulated by reproductive activation and in response to paraquat included prominent members of signalling pathways and anti-oxidants known to affect ageing. Thus, while our results confirm a central role of vitellogenin, they also point to other mechanisms to explain the molecular basis of the lack of a cost of reproduction and the exceptional longevity of social insect reproductives. Thus, socially induced reproductive activation preemptively protects honeybee workers against stressors, explaining their longevity. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'

Larval mortality is the primary symptom of diseased Apis cerana colonies, often attributed to sacbrood virus (SBV) and Melissococcus plutonius. However, the impact of other common honeybee viruses is frequently overlooked, and their pathogenicity to A. cerana remains poorly understood. To investigate the causes of the increasing disease incidence in A. cerana brood, we conducted an epidemiological survey, collecting 70 samples from 19 sites across nine provinces in China. Furthermore, we examined the pathogenicity of Israeli acute paralysis virus (IAPV) in A. cerana brood through artificial inoculation experiments. Our results demonstrate that, besides SBV and M. plutonius, the infection rate and viral load of IAPV in diseased brood are significantly high. Brood artificially inoculated with high concentrations of IAPV exhibited a significant increase in mortality and displayed clinical symptoms similar to those observed in naturally infected colonies. Moreover, a limited resistance to IAPV was observed in A. cerana brood, with some individuals able to restrict viral proliferation. Our study highlights the previously unrecognized pathogenicity of IAPV to A. cerana brood, demonstrating that IAPV poses a significant threat similar to SBV and M. plutonius. We emphasize that IAPV should be recognized as an emerging pathogen causing brood disease in A. cerana and managed accordingly in beekeeping practices.

Interspecies virus transmission involving economically important pollinators, including honey bees ( Apis mellifera ), has recently sparked research interests regarding pollinator health. Given that ants are common pests within apiaries in the southern U.S., the goals of this study were to (1) survey ants found within or near managed honey bee colonies, (2) document what interactions are occurring between ant pests and managed honey bees, and 3) determine if any of six commonly occurring honey bee-associated viruses were present in ants collected from within or far from apiaries. Ants belonging to 14 genera were observed interacting with managed honey bee colonies in multiple ways, most commonly by robbing sugar resources from within hives. We detected at least one virus in 89% of the ant samples collected from apiary sites (n = 57) and in 15% of ant samples collected at non-apiary sites (n = 20). We found that none of these ant samples tested positive for the replication of Deformed wing virus, Black queen cell virus, or Israeli acute paralysis virus, however. Future studies looking at possible virus transmission between ants and bees could determine whether ants can be considered mechanical vectors of honey bee-associated viruses, making them a potential threat to pollinator health.

Abstract Honey bees (Apis mellifera L.) are of undeniable value to agriculture. However, increased mortality of honey bees, mostly due to winter losses associated with parasites and pathogens, have put strain on the apiculture industry. Advancing our knowledge of honey bee viruses and their interactions within the colony environment is vital in mitigating their effect on honey bee health. Our study examined virus sequences detected on beeswax sampled from empty colonies which died during the previous winter. Based on a cage study using virus-containing bees, we confirmed that the introduction of BQCV sequences to wax foundation was possible through workers walking on, and contacting, comb surfaces (worker traffic). Furthermore, we found that BQCV may aerosolize within an incubator to contaminate wax at detectable levels among independent cages. A second cage study explored the potential effects of virus aerosolization on transmission between groups of adult worker bees within cages, having no direct contact. This experiment did not support aerosol transmission between groups of bees in confined spaces. Further work on waxborne virus transmission within colony environments, and potential effects of aerosolization under a wider array of conditions, is crucial to broadening our knowledge of honey bee virus transmission. Our work also highlights potential dangers for beekeepers re-using equipment from dead colonies. Graphical Abstract Graphical Abstract

Insects are often infected with beneficial intracellular bacteria. The bacterium Wolbachia is extremally common in insects and can protect them from pathogenic viruses. Wolbachia is a maternally transmitted bacterium that is widespread in arthropods and filarial nematodes and confers strong antiviral protection in Drosophila melanogaster and other arthropods. Wolbachia -transinfected Aedes aegypti mosquitoes are currently being deployed to fight transmission of dengue and Zika viruses. However, the mechanism of antiviral protection and the factors influencing are still not fully understood. Here, we show that temperature modulates Wolbachia -conferred protection in Drosophila melanogaster . Temperature after infection directly impacts Drosophila C virus (DCV) replication and modulates Wolbachia protection. At higher temperatures, viruses proliferate more and are more lethal, while Wolbachia confers lower protection. Strikingly, host developmental temperature is a determinant of Wolbachia -conferred antiviral protection. While there is strong protection when flies develop from egg to adult at 25°C, the protection is highly reduced or abolished when flies develop at 18°C. However, Wolbachia -induced changes during development are not sufficient to limit virus-induced mortality, as Wolbachia is still required to be present in adults at the time of infection. This developmental effect is general, since it was present in different host genotypes, Wolbachia variants, and upon infection with different viruses. Overall, we show that Wolbachia -conferred antiviral protection is temperature dependent, being present or absent depending on the environmental conditions. This interaction likely impacts Wolbachia -host interactions in nature and, as a result, frequencies of host and symbionts in different climates. Dependence of Wolbachia -mediated pathogen blocking on developmental temperature could be used to dissect the mechanistic bases of protection and influence the deployment of Wolbachia to prevent transmission of arboviruses. IMPORTANCE Insects are often infected with beneficial intracellular bacteria. The bacterium Wolbachia is extremely common in insects and can protect them from pathogenic viruses. This effect is being used to prevent transmission of dengue and Zika viruses by Wolbachia -infected mosquitoes. To understand the biology of insects in the wild, we need to discover which factors affect Wolbachia -conferred antiviral protection. Here, we show that the temperature at which insects develop from eggs to adults can determine the presence or absence of antiviral protection. The environment, therefore, strongly influences this insect-bacterium interaction. Our work may help to provide insights into the mechanism of viral blocking by Wolbachia , deepen our understanding of the geographical distribution of host and symbiont, and incentivize further research on the temperature dependence of Wolbachia- conferred protection for control of mosquito-borne disease.