Deformed wing virus: Difference between revisions

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=1. Classification=
=1. Classification=
==a. Higher order taxa==
==a. Higher order taxa==
Domain: Viruses; Riboviria  
Domain: Viruses; Riboviria  
Kingdom: Orthornaviriae
Kingdom: Orthornaviriae
Phylum: Pisuviricota  
Phylum: Pisuviricota  
Class: Pisoniviricetes  
Class: Pisoniviricetes  
Order: Picornavirales  
Order: Picornavirales  
Family: Iflaviridae  
Family: Iflaviridae  
Genus: Iflavirus
Genus: Iflavirus
Species: Deformed Wing Virus (1).
Species: Deformed Wing Virus (1).


Include this section if your Wiki page focuses on a specific taxon/group of organisms
=2. Description and significance=
=2. Description and significance=
The Deformed Wing Virus (DWV) is a major pathogen for bee species across the world, specifically Apis mellifera. Varroa destructor mites are a common vector of DWV; however, DWV has shown to have a wide range of hosts (2, 3). Infestation of V. destructor mites and DWV increases the incidence of colony collapse disorder (2). DWV is an RNA virus that is known to have several strains, and it is associated with deformities of the wings in some of the infected bees (Figure 1) (3, 4, 2). It is unknown why some bees remain asymptomatic after infection (5). Many colonies that exhibit wing deformities are associated with winter mortality and colony loss (6, 2). DWV is also capable of interacting with various pesticides, potentially causing additional negative effects on bee populations (7). Food transmission is an important method for spreading the virus, since ants consume dead bees, which allows for DWV to disrupt ecosystems (3). Current research involves identifying the virulence of various DWV strains (4). DWV is one of many stressors that has accelerated bee colony loss by causing precocious foraging, increased mortality, deformities, and risk of bees not returning to the hive due to impaired orientation (7).
The Deformed Wing Virus (DWV) is a major pathogen for bee species across the world, specifically Apis mellifera. Varroa destructor mites are a common vector of DWV; however, DWV has shown to have a wide range of hosts (2, 3). Infestation of V. destructor mites and DWV increases the incidence of colony collapse disorder (2). DWV is an RNA virus that is known to have several strains, and it is associated with deformities of the wings in some of the infected bees (Figure 1) (3, 4, 2). It is unknown why some bees remain asymptomatic after infection (5). Many colonies that exhibit wing deformities are associated with winter mortality and colony loss (6, 2). DWV is also capable of interacting with various pesticides, potentially causing additional negative effects on bee populations (7). Food transmission is an important method for spreading the virus, since ants consume dead bees, which allows for DWV to disrupt ecosystems (3). Current research involves identifying the virulence of various DWV strains (4). DWV is one of many stressors that has accelerated bee colony loss by causing precocious foraging, increased mortality, deformities, and risk of bees not returning to the hive due to impaired orientation (7).
=3. Cell structure=
=3. Cell structure=
Organism Key Points
Cell structure:
Cell structure:
DWV has pseudo-T3 icosahedral symmetry. Its structure is composed of three capsid virus proteins: VP1, VP2, and VP3 (8). The VP3 subunit contains a P domain at its core that can attach to different regions of the capsid, due to a flexible 23-residue linker (9). The P domain can adopt conformational changes, and it contains residues that form a catalytic triad: Asp294, His277, and Ser278 (8). The catalytic activity aids the P domain in entering a host’s cell to deliver its genome to the host cell (8). Furthermore, capsids of DWV have spikes around its 5-fold vertices (10). The spikes around the 5-fold vertices are involved in host cell attachment and infection by changing its conformation from an opened to a closed state to release the genome during host entry (10). When the spikes are in its closed conformation, RNA is able to be translocated. This allows the DWV to infect various tissues in bees, particularly in their brain, abdomen, and wings, and in other species, such as Varroa destructor mites (10). The maximum diameter a DWV virion can be is 397Å (8).
DWV has pseudo-T3 icosahedral symmetry. Its structure is composed of three capsid virus proteins: VP1, VP2, and VP3 (8). The VP3 subunit contains a P domain at its core that can attach to different regions of the capsid, due to a flexible 23-residue linker (9). The P domain can adopt conformational changes, and it contains residues that form a catalytic triad: Asp294, His277, and Ser278 (8). The catalytic activity aids the P domain in entering a host’s cell to deliver its genome to the host cell (8). Furthermore, capsids of DWV have spikes around its 5-fold vertices (10). The spikes around the 5-fold vertices are involved in host cell attachment and infection by changing its conformation from an opened to a closed state to release the genome during host entry (10). When the spikes are in its closed conformation, RNA is able to be translocated. This allows the DWV to infect various tissues in bees, particularly in their brain, abdomen, and wings, and in other species, such as Varroa destructor mites (10). The maximum diameter a DWV virion can be is 397Å (8).
=4. Genome structure=
=4. Genome structure=
Genome structure:
Genome structure:
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Pollen has been found to play an important role in inter-taxa virus transmission of DWV. DWV has been observed in a number of additional species such as bumble bees and wasps, which are other pollinating insect species (17). In virus-free colonies, pollen and honey that were infected with DWV were introduced into the hive. After the queen was fed contaminated honey, she became infected and the percentage of eggs infected with DWV increased (17).
Pollen has been found to play an important role in inter-taxa virus transmission of DWV. DWV has been observed in a number of additional species such as bumble bees and wasps, which are other pollinating insect species (17). In virus-free colonies, pollen and honey that were infected with DWV were introduced into the hive. After the queen was fed contaminated honey, she became infected and the percentage of eggs infected with DWV increased (17).
=7. Pathology=
=7. Pathology=
General Pathogenesis
General Pathogenesis:
DWV is often spread by Varroa destructor mites while the mite feeds on honey bee pupae (18, 19). Less frequent infection sources include nurse bees (5), queen ovaries (20, 21) and drone sperm (20, 22). The primary physical manifestation of the virus is, as the name suggests, deformed (stubby and/or useless) wings. The virus also impairs associative learning, memory formation (23), and flight ability (24), induces early foraging (6), and causes premature demise (25). There are suggestions that the younger the larva is in development, the more susceptible it is to negative effects of DWV (5). Physical evidence of horizontal disease transfer (i.e. nurse bees) is not always apparent as the oral infection in larvae is mediated by the amount of virus ingested, and some honey bees are asymptomatic and lived to adulthood (5).
DWV is often spread by Varroa destructor mites while the mite feeds on honey bee pupae (18, 19). Less frequent infection sources include nurse bees (5), queen ovaries (20, 21) and drone sperm (20, 22). The primary physical manifestation of the virus is, as the name suggests, deformed (stubby and/or useless) wings. The virus also impairs associative learning, memory formation (23), and flight ability (24), induces early foraging (6), and causes premature demise (25). There are suggestions that the younger the larva is in development, the more susceptible it is to negative effects of DWV (5). Physical evidence of horizontal disease transfer (i.e. nurse bees) is not always apparent as the oral infection in larvae is mediated by the amount of virus ingested, and some honey bees are asymptomatic and lived to adulthood (5).


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Influence on predators of honeybees:
Influence on predators of honeybees:
Foodborne virus transmission is not a likely transmission source of DWV to bees, yet Myrmica rubra, a scavenger ant that often feeds on dead honeybees, have been found to carry DWV through foodborne transmission (3). Prior research has studied the theory that the range of DWV hosts includes predatory insects, however less work has been published on DWV host potential via foodborne transmission, indicating a need for further inquiry into DWV load in honey bee predators (3).
Foodborne virus transmission is not a likely transmission source of DWV to bees, yet Myrmica rubra, a scavenger ant that often feeds on dead honeybees, have been found to carry DWV through foodborne transmission (3). Prior research has studied the theory that the range of DWV hosts includes predatory insects, however less work has been published on DWV host potential via foodborne transmission, indicating a need for further inquiry into DWV load in honey bee predators (3).
=8. Current Research=
=8. Current Research=
Current Research
Current Research
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The activity and virulence of DWV-A and DWV-B are not fully understood. In a study where DWV-A and DWV-B were both injected into Australian honeybees, the two strains competed, resulting in lower levels of DWV-B compared to when DWV-B was present alone. However, Australian honeybees frequently had higher levels of DWV-B than DWV-A, even when both strains were injected into bees (33). Similar to the findings of Kevill, J. L., et al. (2019), DWV-A had a higher virulence than DWV-B because more Australian honeybees that were injected with DWV-A died compared to those injected with DWV-B and a DWV-recombinant (33).
The activity and virulence of DWV-A and DWV-B are not fully understood. In a study where DWV-A and DWV-B were both injected into Australian honeybees, the two strains competed, resulting in lower levels of DWV-B compared to when DWV-B was present alone. However, Australian honeybees frequently had higher levels of DWV-B than DWV-A, even when both strains were injected into bees (33). Similar to the findings of Kevill, J. L., et al. (2019), DWV-A had a higher virulence than DWV-B because more Australian honeybees that were injected with DWV-A died compared to those injected with DWV-B and a DWV-recombinant (33).
The virulence of DWV-A and DWV-B is not consistent throughout all studies. In another study, where researchers injected DWV-A and DWV-B from the heads of previously infected bees into honey bee pupae, there was no relationship between the strain of DWV and the mortality of pupae (26). When honey bee pupae from Martin Luther University of Halle-Wittenberg were injected with DWV-A and DWV-B, both strains exhibited similar mortality rates, which were higher than controls (36).
The virulence of DWV-A and DWV-B is not consistent throughout all studies. In another study, where researchers injected DWV-A and DWV-B from the heads of previously infected bees into honey bee pupae, there was no relationship between the strain of DWV and the mortality of pupae (26). When honey bee pupae from Martin Luther University of Halle-Wittenberg were injected with DWV-A and DWV-B, both strains exhibited similar mortality rates, which were higher than controls (36).
Author contributions: M.B. wrote the Classification section; K.S. wrote the Introduction section; K.L. wrote the Cell and Genome Structure sections; M.F. wrote the Metabolic Processes and Ecology sections; L.D. wrote the Pathology section; M.B. wrote the Current Research section. M.B. and K.L. curated figures; M.B curated hyperlinks; and M.B., K.L., K.S., and L.D. edited and organized the final article draft.
=9. References=
=9. References=
References
References
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Author contributions: M.B. wrote the Classification section; K.S. wrote the Introduction section; K.L. wrote the Cell and Genome Structure sections; M.F. wrote the Metabolic Processes and Ecology sections; L.D. wrote the Pathology section; M.B. wrote the Current Research section. M.B. and K.L. curated figures; M.B curated hyperlinks; and M.B., K.L., K.S., and L.D. edited and organized the final article draft.
 
<!--Do not edit or remove this line-->[[Category:Pages edited by students of Jennifer
[[Category:Pages edited by students of Jennifer
Bhatnagar at Boston University]]
Bhatnagar at Boston University]]

Latest revision as of 14:51, 7 December 2020

This student page has not been curated.

1. Classification

a. Higher order taxa

Domain: Viruses; Riboviria

Kingdom: Orthornaviriae

Phylum: Pisuviricota

Class: Pisoniviricetes

Order: Picornavirales

Family: Iflaviridae

Genus: Iflavirus

Species: Deformed Wing Virus (1).

2. Description and significance

The Deformed Wing Virus (DWV) is a major pathogen for bee species across the world, specifically Apis mellifera. Varroa destructor mites are a common vector of DWV; however, DWV has shown to have a wide range of hosts (2, 3). Infestation of V. destructor mites and DWV increases the incidence of colony collapse disorder (2). DWV is an RNA virus that is known to have several strains, and it is associated with deformities of the wings in some of the infected bees (Figure 1) (3, 4, 2). It is unknown why some bees remain asymptomatic after infection (5). Many colonies that exhibit wing deformities are associated with winter mortality and colony loss (6, 2). DWV is also capable of interacting with various pesticides, potentially causing additional negative effects on bee populations (7). Food transmission is an important method for spreading the virus, since ants consume dead bees, which allows for DWV to disrupt ecosystems (3). Current research involves identifying the virulence of various DWV strains (4). DWV is one of many stressors that has accelerated bee colony loss by causing precocious foraging, increased mortality, deformities, and risk of bees not returning to the hive due to impaired orientation (7).

3. Cell structure

Cell structure: DWV has pseudo-T3 icosahedral symmetry. Its structure is composed of three capsid virus proteins: VP1, VP2, and VP3 (8). The VP3 subunit contains a P domain at its core that can attach to different regions of the capsid, due to a flexible 23-residue linker (9). The P domain can adopt conformational changes, and it contains residues that form a catalytic triad: Asp294, His277, and Ser278 (8). The catalytic activity aids the P domain in entering a host’s cell to deliver its genome to the host cell (8). Furthermore, capsids of DWV have spikes around its 5-fold vertices (10). The spikes around the 5-fold vertices are involved in host cell attachment and infection by changing its conformation from an opened to a closed state to release the genome during host entry (10). When the spikes are in its closed conformation, RNA is able to be translocated. This allows the DWV to infect various tissues in bees, particularly in their brain, abdomen, and wings, and in other species, such as Varroa destructor mites (10). The maximum diameter a DWV virion can be is 397Å (8).

4. Genome structure

Genome structure: The Deformed Wing Virus (DWV) has a single-stranded positive sense RNA genome, which encodes for a polyprotein responsible for completing the virus’ life cycle, and is flanked by 5’- and 3’- untranslated regions (5). Its genome is 10,140 nucleotides long (8, 12). Nucleotides in the DWV genome can interact with VP3 subunits within the cell (8). The nucleotide sequence of DWV is composed of 29.5% A, 32.3% U, 22.4% G, and 15.8% C content. Amino acid codons in DWV show a preference for U instead of A as the codon’s third base (12). There are three variants of DWV: DWV-A, DWV-B, and DWV-C, with the most virulent types being DWV-A and DWV- B. The internal ribosome entry site, which helps with initiating translation, for DWV-A and DWV-B strains can be found within the first 810 nucleotides (13). Although DWV-A and DWV-B differ in their 5’UTR sequences, 84% of their nucleotides and 95% of their amino acids are shared (14). There are 2,893 polyproteins that are encoded by the single open reading frame (ORF) in the DWV genome. The N terminus is where structural proteins are located, whereas the C terminus is where nonstructural proteins are located (12). One study found that there was no significant difference in the rate of replications amongst the three DWV variants. Whether or not bees are symptomatic is not linked to the genotype of DWV or the transmission route (5). Interesting features of cell structure. Can be combined with “metabolic processes”

5. Metabolic processes

Metabolic processes: The mechanism and process underlying the interaction between the honeybee, mite, and virus are not fully understood, yet immune responses and developmental gene expression observed in honeybees infected with DWV may contribute to the pathogenesis of DWV (15). Honeybees are able to sustain a limited, immediate immune and homeostatic response to DWV. However, these pathways are downregulated shortly after infection, leaving the bee susceptible to viral replication (15). Honeybees infected with DWV-A experience changes in brain gene expression. The expression profile resembles gene expression characteristic of foragers, even in bees too young to begin foraging (16). DWV-A was observed to accelerate honeybee behavioral maturation and initiate molecular pathways in the brain related to the transition from nurse to forager. DWV disrupts transcriptional pathways and is associated with neurogenetic effects such as poor spatial memory and learning deficits (16).

6. Ecology

Ecology: DWV interacts with a neonicotinoid pesticide, thiamethoxam, to influence honeybee health. Bees that are simultaneously exposed to thiamethoxam and DWV do not have a higher viral load compared to bees only exposed to DWV (7). Compared to the controls, honeybees subject to combined exposure of DWV and thiamethoxam have higher mortality rates, engage in precocious foraging, and are less likely to return to the hive after foraging (7). While DWV predominantly affects honeybee populations, additional insect species have been found to be infected by the virus, including the ant species, Myrmica rubra (3). In a sixteen-week feeding experiment, M. rubra were fed honey bee pupae infected with type A and B DWV (3). By the end of the feeding regimen, M. rubra were found to have a high DWV load (3). Pollen has been found to play an important role in inter-taxa virus transmission of DWV. DWV has been observed in a number of additional species such as bumble bees and wasps, which are other pollinating insect species (17). In virus-free colonies, pollen and honey that were infected with DWV were introduced into the hive. After the queen was fed contaminated honey, she became infected and the percentage of eggs infected with DWV increased (17).

7. Pathology

General Pathogenesis: DWV is often spread by Varroa destructor mites while the mite feeds on honey bee pupae (18, 19). Less frequent infection sources include nurse bees (5), queen ovaries (20, 21) and drone sperm (20, 22). The primary physical manifestation of the virus is, as the name suggests, deformed (stubby and/or useless) wings. The virus also impairs associative learning, memory formation (23), and flight ability (24), induces early foraging (6), and causes premature demise (25). There are suggestions that the younger the larva is in development, the more susceptible it is to negative effects of DWV (5). Physical evidence of horizontal disease transfer (i.e. nurse bees) is not always apparent as the oral infection in larvae is mediated by the amount of virus ingested, and some honey bees are asymptomatic and lived to adulthood (5).

Relationship with V. destructor: Prior to global V. destructor population increase, DWV was rarely detected. Now, however, the virus is found in almost all honeybee populations worldwide (27). The V. destructor mite acts as a viral vector; DWV replicates inside V. destructor (5) and while suppressing immune responses (28), the mite feeds on the internal tissues of adult and pupal honeybees allowing the RNA virus to infect the bee (29, 30). In honeybee colonies infected with V. destructor, honeybee pupal mortality is 20% (31, 32). As the remaining honeybees grow to adulthood and V. destructor reproduces in honeybee broods (5), low brood mortality promotes an increasing number of mites and DWV transmission (33).

Influence on predators of honeybees: Foodborne virus transmission is not a likely transmission source of DWV to bees, yet Myrmica rubra, a scavenger ant that often feeds on dead honeybees, have been found to carry DWV through foodborne transmission (3). Prior research has studied the theory that the range of DWV hosts includes predatory insects, however less work has been published on DWV host potential via foodborne transmission, indicating a need for further inquiry into DWV load in honey bee predators (3).

8. Current Research

Current Research Current research focuses on the different strains of Deformed Wing Virus, specifically understanding the prevalence and mortality rates associated with DWV-A, DWV-B, and DWV-C. In one study, honeybee colonies were collected from England, Wales, and 32 states from the United States, to better understand how the different strains of DWV impact colonies from these regions. Of the survivors from the spring and fall collections taken from England and Wales, there was a higher load of DWV-B than DWV-A, and DWV-C had the lowest load (4). Of the colonies that died, a larger portion of bees were contaminated with DWV-A than DWV-B. DWV-C had the lowest virulence of the three strains (4). Regarding collections from the United States, DWV-A was the most common strain found within colonies, but levels of DWV-B are increasing in beehives (4), and the United States has more overwinter colony loss than England (34, 35). The activity and virulence of DWV-A and DWV-B are not fully understood. In a study where DWV-A and DWV-B were both injected into Australian honeybees, the two strains competed, resulting in lower levels of DWV-B compared to when DWV-B was present alone. However, Australian honeybees frequently had higher levels of DWV-B than DWV-A, even when both strains were injected into bees (33). Similar to the findings of Kevill, J. L., et al. (2019), DWV-A had a higher virulence than DWV-B because more Australian honeybees that were injected with DWV-A died compared to those injected with DWV-B and a DWV-recombinant (33). The virulence of DWV-A and DWV-B is not consistent throughout all studies. In another study, where researchers injected DWV-A and DWV-B from the heads of previously infected bees into honey bee pupae, there was no relationship between the strain of DWV and the mortality of pupae (26). When honey bee pupae from Martin Luther University of Halle-Wittenberg were injected with DWV-A and DWV-B, both strains exhibited similar mortality rates, which were higher than controls (36).


Author contributions: M.B. wrote the Classification section; K.S. wrote the Introduction section; K.L. wrote the Cell and Genome Structure sections; M.F. wrote the Metabolic Processes and Ecology sections; L.D. wrote the Pathology section; M.B. wrote the Current Research section. M.B. and K.L. curated figures; M.B curated hyperlinks; and M.B., K.L., K.S., and L.D. edited and organized the final article draft.

9. References

References [1.] NCBI. (2020) Taxonomy Browser (Deformed Wing Virus). National Center for Biotechnology Information. U.S. National Library of Medicine.

[2.] Brettell, L., et al. (2017). A Comparison of Deformed Wing Virus in Deformed and Asymptomatic Honey Bees. Insects, 8: 28.

[3.] Schlappi, L., et al. (2019). Foodborne transmission of deformed wing virus to ants (Myrmica rubra). Insects, 10: 394.

[4.] Kevill, J. L., et al. (2019). DWV-A lethal to honey bees (Apis mellifera): a colony level survey of DWV variants (A, B, and C) in England, Wales, and 32 States across the US. Viruses, 11: 426.

[5] Gusachenko, O.N., et al. (2020). Green Bees: Reverse Genetic Analysis of Deformed Wing Virus Transmission, Replication, and Tropism. Viruses, 12: 532.

[6] Benaets, K., et al. (2017). Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proceedings of the Royal Society of London, Biological Sciences, 284: 20162149.

[7] Coulon, M., et al. (2020). Interactions between thiamethoxam and deformed wing virus can drastically impair flight behavior of honey bees. Frontiers in Microbiology, 11: 766.

[8] Škubník, K., et al. (2017). Structure of deformed wing virus, a major honey bee pathogen. Proceedings of the National Academy of Sciences - PNAS, 114: 3210-3215.

[9] Kalynych, S., et al. (2016). Virion Structure of Iflavirus Slow Bee Paralysis Virus at 2.6-Angstrom Resolution. Journal of Virology, 90: 7444-7455.

[10] Organtini, L., et al. (2017). Honey Bee Deformed Wing Virus Structures Reveal that Conformational Changes Accompany Genome Release. Journal of Virology, 91: 01795-16.

[11] Lamp, B., et al. (2016). Construction and Rescue of a Molecular Clone of Deformed Wing Virus (DWV). PloS One, 11: 11.

[12] Lanzi, G., et al. (2006). Molecular and Biological Characterization of Deformed Wing Virus of Honeybees (Apis mellifera L.). Journal of Virology, 80: 4998-5009.

[13] Ongus, J.R., et al. (2006). The 5’ non-translated region of Varroa destructor virus 1 (genus Iflavirus): structure prediction and IRES activity in Lymantria dispar cells. Journal of General Virology, 87: 3397–3407.

[14] Ongus, J.R., et al. (2004). Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. Journal of General Virology, 85: 3747–3755.

[15] Zhao, Y., et al. (2019). The Dynamics of Deformed Wing Virus Concentration and Host Defensive Gene Expression after Varroa Mite Parasitism in Honey Bees, Apis mellifera. Insects, 10: 16.

[16] Traniello, I. M., et al. (2020). Meta-analysis of honey bee neurogenomic response links Deformed wing virus type A to precocious behavioral maturation. Scientific Reports, 10: 3101.

[17.] Singh, R., et al. (2010). RNA viruses in hymenopteran pollinators: evidence of inter-Taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PloS one, 5: 14357.

[18.] de Miranda, J. R., and Genersch, E. (2010). Deformed wing virus. Journal of Invertebrate Pathology, 103: S48-61.

[19.] Möckel, N., et al. (2011). Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. Journal of General Virology, 92: 370-77.

[20.] Yue, C., et al. (2007). Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). Journal of General Virology, 88: 2329-36.

[21.] Amiri, E., et al. (2018). Quantitative patterns of vertical transmission of deformed wing virus in honey bees. Public Library of Science, One, 13: e0195283.

[22.] Amiri, E., et al. (2016). Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Scientific Reports, 6: 33065.

[23.] Iqbal, J., and Mueller, U. (2007). Virus infection causes specific learning deficits in honeybee foragers. Proceedings of the Royal Society of London, Biology, 274: 1517-21.

[24.] Wells, T., et al. (2016). Flight performance of actively foraging honey bees is reduced by a common pathogen. Environmental Microbiology Reports, 8: 728-37.

[25.] Dainat B., et al. (2012). Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Applied and Environmental Microbiology, 78: 981-7.

[26.] Dubois, E., et al. (2019). Outcomes of honeybee pupae inoculated with deformed wing virus genotypes A and B. Apidologie, 51:18-34.

[27.] Roberts, J.M., et al. (2017). Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Scientific Reports, 7: 6925.

[28.] Yang, X., and Cox-Foster, D.L. (2005). Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences of the USA, 102: 7470-5.

[29.] Rosenkranz, P., et al. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103: S96-119.

[30.] Le Conte, Y., et al. (2010). Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie, 41: 353-63.

[31.] Martin, S. J. (2001). The role of Varroa and viral pathogens in the collapse of honey bee colonies: a modelling approach. Journal of Applied Ecology, 38: 1082-93.

[32.] Martin, S. J., et al. (2013). The role of deformed wing virus in the initial collapse of Varroa infested honey bee colonies in the UK. Journal of Apicultural Research, 52: 521-8.

[33.] Norton, A. M., et al. (2020). Accumulation and competition amongst deformed wing virus genotypes in naive Australian honeybees provides insight into increasing global prevalence of Genotype B. Frontiers in Microbiology, 11: 620.

[34.] Bee Informed Partnership (2016–2017). Loss Results. Bee Informed. https://beeinformed.org/2017/05/25/2016-2017-loss-results-thank-you-to-all-survey-participants/(accessed on 14 September 2020).

[35.] Winter Survival Survey (2017). The British Beekeepers Association. https://www.bbka.org.uk/winter-honey-bee-losses-in-england. (accessed on 14 September 2020).

[36.] Tehel, A., et al. (2019). The two prevalent genotypes of an emerging infectious disease, deformed wing virus, cause equally low pupal mortality and equally high wing deformities in host honey bees. Viruses, 11: 114.


[[Category:Pages edited by students of Jennifer Bhatnagar at Boston University]]