RNAseq Analysis Reveals Virus Diversity within Hawaiian Apiary Insect Communities

Deformed wing virus (DWV) is the most abundant viral pathogen of honey bees and has been associated with large-scale colony losses. DWV and other bee-associated RNA viruses are generalists capable of infecting diverse hosts. Here, we used RNAseq analysis to test the hypothesis that due to the frequency of interactions, a range of apiary pest species would become infected with DWV and/or other honey bee-associated viruses. We confirmed that DWV-A was the most prevalent virus in the apiary, with genetically similar sequences circulating in the apiary pests, suggesting frequent inter-species transmission. In addition, different proportions of the three DWV master variants as indicated by BLAST analysis and genome coverage plots revealed interesting DWV-species groupings. We also observed that new genomic recombinants were formed by the DWV master variants, which are likely adapted to replicate in different host species. Species groupings also applied when considering other viruses, many of which were widespread in the apiaries. In social wasps, samples were grouped further by site, which potentially also influenced viral load. Thus, the apiary invertebrate community has the potential to act as reservoirs of honey bee-associated viruses, highlighting the importance of considering the wider community in the apiary when considering honey bee health.

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Haemolymph removal by the parasite Varroa destructor can trigger the proliferation of the Deformed Wing Virus in mite infested bees (Apis mellifera), contributing to enhanced pathogen virulence

10.1101/257667 ◽

2018 ◽

Cited By ~ 6

Author(s):

Desiderato Annoscia ◽

Sam P. Brown ◽

Gennaro Di Prisco ◽

Emanuele De Paoli ◽

Simone Del Fabbro ◽

...

Keyword(s):

Honey Bee ◽

Varroa Destructor ◽

Viral Evolution ◽

Colony Losses ◽

Viral Pathogen ◽

Deformed Wing Virus ◽

Bee Colony ◽

Bee Health ◽

Honey Bee Health ◽

Mite Feeding

AbstractThe association between the Deformed Wing Virus and the parasitic mite Varroa destructor has been identified as a major cause of worldwide honey bee colony losses. The mite acts as a vector of the viral pathogen and can trigger its replication in infected bees. However, the mechanistic details underlying this tripartite interaction are still poorly defined, and, in particular, the causes of viral proliferation in mite infested bees.Here we develop and test a novel hypothesis - grounded in ecological predator-prey theory - that mite feeding destabilizes viral immune control through the removal of both viral ‘prey’ and immune ‘predators’, triggering uncontrolled viral replication. Consistent with this hypothesis, we show that experimental removal of increasing volumes of haemolymph from individual bees results in increasing viral densities. In contrast, we find no support for alternative proposed mechanisms of viral expansion via mite immune-suppression or within-host viral evolution.Overall, these results provide a new model for the mechanisms driving pathogen-parasite interactions in bees, which ultimately underpin honey bee health decline and colony losses.

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Tolerance of Honey Bees to Varroa Mite in the Absence of Deformed Wing Virus

Viruses ◽

10.3390/v12050575 ◽

2020 ◽

Vol 12 (5) ◽

pp. 575 ◽

Cited By ~ 3

Author(s):

John M. K. Roberts ◽

Nelson Simbiken ◽

Chris Dale ◽

Joel Armstrong ◽

Denis L. Anderson

Keyword(s):

Honey Bee ◽

Honey Bees ◽

High Throughput Sequencing ◽

Solomon Islands ◽

Host Shift ◽

Colony Losses ◽

Viral Pathogen ◽

Deformed Wing Virus ◽

Bee Health ◽

Queen Cell

The global spread of the parasitic mite Varroa destructor has emphasized the significance of viruses as pathogens of honey bee (Apis mellifera) populations. In particular, the association of deformed wing virus (DWV) with V. destructor and its devastating effect on honey bee colonies has led to that virus now becoming one of the most well-studied insect viruses. However, there has been no opportunity to examine the effects of Varroa mites without the influence of DWV. In Papua New Guinea (PNG), the sister species, V. jacobsoni, has emerged through a host-shift to reproduce on the local A. mellifera population. After initial colony losses, beekeepers have maintained colonies without chemicals for more than a decade, suggesting that this bee population has an unknown mite tolerance mechanism. Using high throughput sequencing (HTS) and target PCR detection, we investigated whether the viral landscape of the PNG honey bee population is the underlying factor responsible for mite tolerance. We found A. mellifera and A. cerana from PNG and nearby Solomon Islands were predominantly infected by sacbrood virus (SBV), black queen cell virus (BQCV) and Lake Sinai viruses (LSV), with no evidence for any DWV strains. V. jacobsoni was infected by several viral homologs to recently discovered V. destructor viruses, but Varroa jacobsoni rhabdovirus-1 (ARV-1 homolog) was the only virus detected in both mites and honey bees. We conclude from these findings that A. mellifera in PNG may tolerate V. jacobsoni because the damage from parasitism is significantly reduced without DWV. This study also provides further evidence that DWV does not exist as a covert infection in all honey bee populations, and remaining free of this serious viral pathogen can have important implications for bee health outcomes in the face of Varroa.

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The Gut Microbiota Can Provide Viral Tolerance in the Honey Bee

Microorganisms ◽

10.3390/microorganisms9040871 ◽

2021 ◽

Vol 9 (4) ◽

pp. 871

Author(s):

Christopher Dosch ◽

Anja Manigk ◽

Tabea Streicher ◽

Anja Tehel ◽

Robert J. Paxton ◽

...

Keyword(s):

Gut Microbiota ◽

Honey Bee ◽

Honey Bees ◽

Negative Effects ◽

Positive Role ◽

Viral Pathogen ◽

Deformed Wing Virus ◽

Bee Health ◽

Honey Bee Health

Adult honey bees host a remarkably consistent gut microbial community that is thought to benefit host health and provide protection against parasites and pathogens. Currently, however, we lack experimental evidence for the causal role of the gut microbiota in protecting the Western honey bees (Apis mellifera) against their viral pathogens. Here we set out to fill this knowledge gap by investigating how the gut microbiota modulates the virulence of a major honey bee viral pathogen, deformed wing virus (DWV). We found that, upon oral virus exposure, honey bee survival was significantly increased in bees with an experimentally established normal gut microbiota compared to control bees with a perturbed (dysbiotic) gut microbiota. Interestingly, viral titers were similar in bees with normal gut microbiota and dysbiotic bees, pointing to higher viral tolerance in bees with normal gut microbiota. Taken together, our results provide evidence for a positive role of the gut microbiota for honey bee fitness upon viral infection. We hypothesize that environmental stressors altering honey bee gut microbiota composition, e.g., antibiotics in beekeeping or pesticides in modern agriculture, could interact synergistically with pathogens, leading to negative effects on honey bee health and the epidemiology and impact of their viruses.

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Comb Irradiation Has Limited, Interactive Effects on Colony Performance or Pathogens in Bees, Varroa destructor and Wax Based on Two Honey Bee Stocks

Insects ◽

10.3390/insects10010015 ◽

2019 ◽

Vol 10 (1) ◽

pp. 15 ◽

Cited By ~ 2

Author(s):

Lilia I. De Guzman ◽

Michael Simone-Finstrom ◽

Amanda M. Frake ◽

Philip Tokarz

Keyword(s):

Honey Bee ◽

Honey Bees ◽

Varroa Destructor ◽

Adult Population ◽

Interactive Effects ◽

Colony Losses ◽

Deformed Wing Virus ◽

Bee Health ◽

Honey Bee Health ◽

Russian Honey Bees

Parasitic mites and pathogens compromise honey bee health. Development of sustainable and integrative methods of managing these problems will minimize their detrimental impact on honey bees. Here, we aimed to determine if the combination of using mite-resistant stocks along with gamma-irradiated combs influences colony health and productivity. The major finding concerned honey bee genotype confirming that Russian honey bees are more resistant to Varroa destructor than Italian honey bees. The effect of comb irradiation was inconsistent showing a significant increase in adult bee population and amount of stored pollen in 2015, but not in 2016. The increased amount of stored pollen was probably associated with larger adult population in colonies with irradiated combs in September 2015 regardless of honey bee stock. Nevertheless, the ability of bees to collect and store more pollen in the irradiated group does not appear to compensate the negative impacts of mite parasitism on honey bees especially in the Italian bees, which consistently suffered significant colony losses during both years. Results of viral analyses of wax, newly emerged bees, and Varroa and their pupal hosts showed common detections of Deformed wing virus (DWV), Varroa destructor virus (VDV-1), Chronic bee paralysis virus (CBPV), and Black queen cell virus (BQCV). Wax samples had on average ~4 viruses or pathogens detected in both irradiated and non-irradiated combs. Although pathogen levels varied by month, some interesting effects of honey bee stock and irradiation treatment were notable, indicating how traits of mite resistance and alternative treatments may have additive effects. Further, this study indicates that wax may be a transmission route of viral infection. In addition, pupae and their infesting mites from Italian colonies exhibited higher levels of DWV than those from Russian colonies suggesting potential DWV resistance by Russian honey bees. CBPV levels were also reduced in mites from Russian colonies in general and in mites, mite-infested pupae, and newly emerged bees that were collected from irradiated combs. However, BQCV levels were not reduced by comb irradiation. Overall, the contribution of irradiating comb in improving honey bee health and colony survival appears to be subtle, but may be useful as part of an integrated pest management strategy with the addition of using mite-resistant stocks.

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Impact of Chronic Exposure to Sublethal Doses of Glyphosate on Honey Bee Immunity, Gut Microbiota and Infection by Pathogens

Microorganisms ◽

10.3390/microorganisms9040845 ◽

2021 ◽

Vol 9 (4) ◽

pp. 845

Author(s):

Loreley Castelli ◽

Sofía Balbuena ◽

Belén Branchiccela ◽

Pablo Zunino ◽

Joanito Liberti ◽

...

Keyword(s):

Gut Microbiota ◽

Honey Bee ◽

Chronic Exposure ◽

Pollination Services ◽

Deformed Wing Virus ◽

Immune Genes ◽

Bee Health ◽

Honey Bee Health ◽

Sublethal Doses ◽

The Impact

Glyphosate is the most used pesticide around the world. Although different studies have evidenced its negative effect on honey bees, including detrimental impacts on behavior, cognitive, sensory and developmental abilities, its use continues to grow. Recent studies have shown that it also alters the composition of the honey bee gut microbiota. In this study we explored the impact of chronic exposure to sublethal doses of glyphosate on the honey bee gut microbiota and its effects on the immune response, infection by Nosema ceranae and Deformed wing virus (DWV) and honey bee survival. Glyphosate combined with N. ceranae infection altered the structure and composition of the honey bee gut microbiota, for example by decreasing the relative abundance of the core members Snodgrassella alvi and Lactobacillus apis. Glyphosate increased the expression of some immune genes, possibly representing a physiological response to mitigate its negative effects. However, this response was not sufficient to maintain honey bee health, as glyphosate promoted the replication of DWV and decreased the expression of vitellogenin, which were accompanied by a reduced life span. Infection by N. ceranae also alters honey bee immunity although no synergistic effect with glyphosate was observed. These results corroborate previous findings suggesting deleterious effects of widespread use of glyphosate on honey bee health, and they contribute to elucidate the physiological mechanisms underlying a global decline of pollination services.

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Descriptive Analysis of the Varroa Non-Reproduction Trait in Honey Bee Colonies and Association with Other Traits Related to Varroa Resistance

Insects ◽

10.3390/insects11080492 ◽

2020 ◽

Vol 11 (8) ◽

pp. 492 ◽

Cited By ~ 1

Author(s):

Sonia E. Eynard ◽

Christina Sann ◽

Benjamin Basso ◽

Anne-Laure Guirao ◽

Yves Le Conte ◽

...

Keyword(s):

Honey Bee ◽

Empirical Bayes ◽

Descriptive Analysis ◽

Field Studies ◽

Colony Losses ◽

Bee Colony ◽

Bee Health ◽

Honey Bee Health ◽

Varroa Resistance ◽

Resistance Traits

In the current context of worldwide honey bee colony losses, among which the varroa mite plays a major role, the hope to improve honey bee health lies in part in the breeding of varroa resistant colonies. To do so, methods used to evaluate varroa resistance need better understanding. Repeatability and correlations between traits such as mite non-reproduction (MNR), varroa sensitive hygiene (VSH), and hygienic behavior are poorly known, due to practical limitations and to their underlying complexity. We investigate (i) the variability, (ii) the repeatability of the MNR score, and (iii) its correlation with other resistance traits. To reduce the inherent variability of MNR scores, we propose to apply an empirical Bayes correction. In the short-term (ten days), MNR had a modest repeatability of 0.4, whereas in the long-term (a month), it had a low repeatability of 0.2, similar to other resistance traits. Within our dataset, there was no correlation between MNR and VSH. Although MNR is amongst the most popular varroa resistance estimates in field studies, its underlying complex mechanism is not fully understood. Its lack of correlation with better described resistance traits and low repeatability suggest that MNR needs to be interpreted cautiously, especially when used for selection.

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Deformed Wing Virus Infection in Honey Bees (Apis mellifera L.)

Veterinary Pathology ◽

10.1177/0300985819834617 ◽

2019 ◽

Vol 56 (4) ◽

pp. 636-641 ◽

Cited By ~ 5

Author(s):

Roman V. Koziy ◽

Sarah C. Wood ◽

Ivanna V. Kozii ◽

Claire Janse van Rensburg ◽

Igor Moshynskyy ◽

...

Keyword(s):

Apis Mellifera ◽

Honey Bee ◽

Honey Bees ◽

Rna Virus ◽

Mandibular Glands ◽

Deformed Wing Virus ◽

Clinically Normal ◽

Bee Health ◽

Honey Bee Health ◽

Honey Bee Workers

Deformed wing virus (DWV) is a single-stranded RNA virus of honey bees ( Apis mellifera L.) transmitted by the parasitic mite Varroa destructor. Although DWV represents a major threat to honey bee health worldwide, the pathological basis of DWV infection is not well documented. The objective of this study was to investigate clinicopathological and histological aspects of natural DWV infection in honey bee workers. Emergence of worker honey bees was observed in 5 colonies that were clinically affected with DWV and the newly emerged bees were collected for histopathology. DWV-affected bees were 2 times slower to emerge and had 30% higher mortality compared to clinically normal bees. Hypopharyngeal glands in bees with DWV were hypoplastic, with fewer intracytoplasmic secretory vesicles; cells affected by apoptosis were observed more frequently. Mandibular glands were hypoplastic and were lined by cuboidal epithelium in severely affected bees compared to tall columnar epithelium in nonaffected bees. The DWV load was on average 1.7 × 106 times higher ( P < .001) in the severely affected workers compared to aged-matched sister honey bee workers that were not affected by deformed wing disease based on gross examination. Thus, DWV infection is associated with prolonged emergence, increased mortality during emergence, and hypoplasia of hypopharyngeal and mandibular glands in newly emerged worker honey bees in addition to previously reported deformed wing abnormalities.

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A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1523515113 ◽

2016 ◽

Vol 113 (12) ◽

pp. 3203-3208 ◽

Cited By ~ 101

Author(s):

Gennaro Di Prisco ◽

Desiderato Annoscia ◽

Marina Margiotta ◽

Rosalba Ferrara ◽

Paola Varricchio ◽

...

Keyword(s):

Honey Bee ◽

Stress Factors ◽

Colony Losses ◽

Viral Pathogen ◽

Deformed Wing Virus ◽

Mutualistic Symbiosis ◽

Bee Colony ◽

Parasitic Mite ◽

Honey Bee Colony ◽

Honey Bee Colony Losses

Honey bee colony losses are triggered by interacting stress factors consistently associated with high loads of parasites and/or pathogens. A wealth of biotic and abiotic stressors are involved in the induction of this complex multifactorial syndrome, with the parasitic mite Varroa destructor and the associated deformed wing virus (DWV) apparently playing key roles. The mechanistic basis underpinning this association and the evolutionary implications remain largely obscure. Here we narrow this research gap by demonstrating that DWV, vectored by the Varroa mite, adversely affects humoral and cellular immune responses by interfering with NF-κB signaling. This immunosuppressive effect of the viral pathogen enhances reproduction of the parasitic mite. Our experimental data uncover an unrecognized mutualistic symbiosis between Varroa and DWV, which perpetuates a loop of reciprocal stimulation with escalating negative effects on honey bee immunity and health. These results largely account for the remarkable importance of this mite–virus interaction in the induction of honey bee colony losses. The discovery of this mutualistic association and the elucidation of the underlying regulatory mechanisms sets the stage for a more insightful analysis of how synergistic stress factors contribute to colony collapse, and for the development of new strategies to alleviate this problem.

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Impacts of Diverse Natural Products on Honey Bee Viral Loads and Health

Applied Sciences ◽

10.3390/app112210732 ◽

2021 ◽

Vol 11 (22) ◽

pp. 10732

Author(s):

Dawn L. Boncristiani ◽

James P. Tauber ◽

Evan C. Palmer-Young ◽

Lianfei Cao ◽

William Collins ◽

...

Keyword(s):

Natural Products ◽

Immune Responses ◽

Honey Bee ◽

Honey Bees ◽

Food Sources ◽

Deformed Wing Virus ◽

Bee Health ◽

Honey Bee Health ◽

Living Organisms ◽

Bee Disease

Western honey bees (Apis mellifera), a cornerstone to crop pollination in the U.S., are faced with an onslaught of challenges from diseases caused by parasites, pathogens, and pests that affect this economically valuable pollinator. Natural products (NPs), produced by living organisms, including plants and microorganisms, can support health and combat disease in animals. NPs include both native extracts and individual compounds that can reduce disease impacts by supporting immunity or directly inhibiting pathogens, pests, and parasites. Herein, we describe the screening of NPs in laboratory cage studies for their effects on honey bee disease prevention and control. Depending on the expected activity of compounds, we measured varied responses, including viral levels, honey bee immune responses, and symbiotic bacteria loads. Of the NPs screened, several compounds demonstrated beneficial activities in honey bees by reducing levels of the critical honey bee virus deformed wing virus (DWV-A and-B), positively impacting the gut microbiome or stimulating honey bee immune responses. Investigations of the medicinal properties of NPs in honey bees will contribute to a better understanding of their potential to support honey bee immunity to fight off pests and pathogens and promote increased overall honey bee health. These investigations will also shed light on the ecological interactions between pollinators and specific floral food sources.

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Occurrence and Molecular Phylogeny of Honey Bee Viruses in Vespids

Viruses ◽

10.3390/v12010006 ◽

2019 ◽

Vol 12 (1) ◽

pp. 6 ◽

Cited By ~ 1

Author(s):

Sa Yang ◽

Philippe Gayral ◽

Hongxia Zhao ◽

Yaojun Wu ◽

Xuejian Jiang ◽

...

Keyword(s):

Honey Bee ◽

Phylogenetic Analyses ◽

Virus Transmission ◽

Deformed Wing Virus ◽

Two Samples ◽

Bee Health ◽

Queen Cell ◽

Honey Bee Health ◽

Infection Processes ◽

Bee Viruses

Since the discovery that honey bee viruses play a role in colony decline, researchers have made major breakthroughs in understanding viral pathology and infection processes in honey bees. Work on virus transmission patterns and virus vectors, such as the mite Varroa destructor, has prompted intense efforts to manage honey bee health. However, little is known about the occurrence of honey bee viruses in bee predators, such as vespids. In this study, we characterized the occurrence of 11 honey bee viruses in five vespid species and one wasp from four provinces in China and two vespid species from four locations in France. The results showed that all the species from China carried certain honey bee viruses, notably Apis mellifera filamentous virus (AmFV), Deformed wing virus (DWV), and Israeli acute paralysis virus (IAPV); furthermore, in some vespid colonies, more than three different viruses were identified. In France, DWV was the most common virus; Sacbrood virus (SBV) and Black queen cell virus (BQCV) were observed in one and two samples, respectively. Phylogenetic analyses of IAPV and BQCV sequences indicated that most of the IAPV sequences belonged to a single group, while the BQCV sequences belonged to several groups. Additionally, our study is the first to detect Lake Sinai virus (LSV) in a hornet from China. Our findings can guide further research into the origin and transmission of honey bee viruses in Vespidae, a taxon of ecological, and potentially epidemiological, relevance.

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