1932

Abstract

Deformed wing virus (DWV) has become the most well-known, widespread, and intensively studied insect pathogen in the world. Although DWV was previously present in honeybee populations, the arrival and global spread of a new vector, the ectoparasitic mite , has dramatically altered DWV epidemiology. DWV is now the most prevalent virus in honeybees, with a minimum average of 55% of colonies/apiaries infected across 32 countries. Additionally, DWV has been detected in 65 arthropod species spanning eight insect orders and three orders of Arachnida. Here, we describe the significant progress that has been made in elucidating the capsid structure of the virus, understanding its ever-expanding host range, and tracking the constantly evolving DWV genome and formation of recombinants. The construction of molecular clones, working with DWV in cell lines, and the development of immunohistochemistry methods will all help the community to move forward. Identifying the tissues in which DWV variants are replicating and understanding the impact of DWV in non-honeybee hosts are major new goals.

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2019-09-29
2024-07-20
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Literature Cited

  1. 1. 
    Bowen-Walker PL, Martin SJ, Gunn A 1999. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J. Invertebr. Pathol. 73:101–6
    [Google Scholar]
  2. 2. 
    Highfield AC, El Nagar A, Mackinder LCM, Laure M-L, Hall MJ et al. 2009. Deformed wing virus implicated in overwintering honeybee colony losses. Appl. Environ. Microbiol. 75:7212–20
    [Google Scholar]
  3. 3. 
    Schroeder DC, Martin SJ. 2012. Deformed wing virus: the main suspect in unexplained honeybee deaths worldwide. Virulence 3:589–91
    [Google Scholar]
  4. 4. 
    Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P 2012. Predictive markers of honey bee colony collapse. PLOS ONE 7:e32151
    [Google Scholar]
  5. 5. 
    Francis RM, Nielsen SL, Kryger P 2013. Varroa-virus interaction in collapsing honey bee colonies. PLOS ONE 8:e57540
    [Google Scholar]
  6. 6. 
    Mondet F, de Miranda JR, Kretzschmar A, Le Conte Y, Mercer AR 2014. On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLOS Pathog 10:e1004323
    [Google Scholar]
  7. 7. 
    Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE et al. 2012. Global honey bee viral landscape altered by a parasitic mite. Science 336:1304–6
    [Google Scholar]
  8. 8. 
    Ryabov EV, Wood GR, Fannon JM, Moore JD, Bull JC et al. 2014. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLOS Path 10:e1004230
    [Google Scholar]
  9. 9. 
    Wilfert L, Long G, Leggett HC, Schmid-Hempel P, Butlin R et al. 2016. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351:594–97
    [Google Scholar]
  10. 10. 
    Fürst MA, McMahon DP, Osborne JL, Paxton RJ, Brown MJF 2014. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:7488364–66
    [Google Scholar]
  11. 11. 
    Santamaria J, Villalobos EM, Brettell LE, Nikaido S, Graham JR, Martin SJ 2017. Evidence of Varroa-mediated deformed wing virus spillover in Hawaii. J. Invertebr. Pathol. 151:126–30
    [Google Scholar]
  12. 12. 
    de Miranda JR, Genersch E 2010. Deformed wing virus. J. Invertebr. Pathol. 103:S48–61
    [Google Scholar]
  13. 13. 
    Genersch E, Aubert M. 2010. Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet. Res. 41:54
    [Google Scholar]
  14. 14. 
    Grozinger CM, Flenniken ML. 2019. Bee viruses: ecology, pathogenicity, and impacts. Annu. Rev. Entomol. 64:205–26
    [Google Scholar]
  15. 15. 
    Nazzi F, Conte YL. 2016. Ecology of Varroa destructor, the major ectoparasite of the Western honey bee, Apis mellifera. Annu. Rev. Entomol. 61:417–32
    [Google Scholar]
  16. 16. 
    Nazzi F, Pennacchio F. 2018. Honey bee antiviral immune barriers as affected by multiple stress factors: a novel paradigm to interpret colony health decline and collapse. Viruses 10:159
    [Google Scholar]
  17. 17. 
    Bailey L, Ball BV. 1991. Honey Bee Pathology London: Academic, 2nd ed..
    [Google Scholar]
  18. 18. 
    Allen M, Ball B. 1996. The incidence and world distribution of honey bee viruses. Bee World 77:141–62
    [Google Scholar]
  19. 19. 
    Carreck NL, Ball BV, Martin SJ 2010. Honey bee colony collapse and changes in viral prevalence associated with Varroa destructor. J. Apic. Res 49:93–94
    [Google Scholar]
  20. 20. 
    de Miranda JR, Bailey L, Ball BV, Blanchard P, Budge GE et al. 2013. Standard methods for virus research in Apis mellifera. J. Apic. Res 52:41–56
    [Google Scholar]
  21. 21. 
    Martin SJ, Ball BV, Carreck NL 2010. Prevalence and persistence of deformed wing virus (DWV) in untreated or acaricide-treated Varroa destructor infested honey bee (Apis mellifera L.) colonies. J. Apic. Res. 49:72–79
    [Google Scholar]
  22. 22. 
    Kajobe R, Marris G, Budge G, Laurenson L, Cordoni G et al. 2010. First molecular detection of a viral pathogen in Ugandan honey bees. J. Invertebr. Pathol. 104:153–56
    [Google Scholar]
  23. 23. 
    Roberts JM, Anderson DL, Durr PA 2017. Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Sci. Rep. 7:6925
    [Google Scholar]
  24. 24. 
    Shutler D, Head K, Burgher-MacLellan KL, Colwell MJ, Levitt AL et al. 2014. Honey bee Apis mellifera parasites in the absence of Nosema cerana fungi and Varroa destructor mites. PLOS ONE 9:e98599
    [Google Scholar]
  25. 25. 
    Berényi O, Bakonyi T, Derakhshifar I, Köglberger H, Nowotny N 2006. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl. Environ. Microbiol. 72:2414–20
    [Google Scholar]
  26. 26. 
    Griffiths DA, Bowman CE. 1981. World distribution of the mite Varroa jacobsoni, a parasite of honeybees. Bee World 62:154–63
    [Google Scholar]
  27. 27. 
    Boncristiani H, Li J, Evans JD, Pettis J, Chen Y 2011. Scientific note on PCR inhibitors in the compound eyes of honey bees, Apis mellifera. Apidologie 42:457–60
    [Google Scholar]
  28. 28. 
    Lanzi G, de Miranda JR, Boniotti MB, Cameron CE, Lavazza A et al. 2006. Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). J. Virol. 80:4998–5009
    [Google Scholar]
  29. 29. 
    Ongus JR, Roode EC, Pleij CWA, Vlak JM, van Oers MM 2006. The 5′ non-translated region of Varroa destructor virus-1 (genus Iflavirus): structure prediction and IRES activity in Lymantria dispar cells. J. Gen. Virol. 87:3397–407
    [Google Scholar]
  30. 30. 
    van Oers MM. 2010. Genomics and biology of Iflaviruses. Insect Virology S Asgari, K Johnson 231–50 Norfolk, UK: Caister Academic
    [Google Scholar]
  31. 31. 
    Sánchez-Eugenia R, Goikolea J, Gil-Cartón D, Sánchez-Magraner L, Guérin DMA 2015. Triatoma virus recombinant VP4 protein induces membrane permeability through dynamic pores. J. Virol. 89:4645–54
    [Google Scholar]
  32. 32. 
    Škubník K, Nováček J, Füzik T, Přidal A, Paxton RJ, Plevka P 2017. Structure of deformed wing virus, a major honey bee pathogen. PNAS 114:3210–15
    [Google Scholar]
  33. 33. 
    Organtini LJ, Shingler KL, Ashley RE, Capaldi EA, Durrani K et al. 2017. Honey bee deformed wing virus structures reveal that conformational changes accompany genome release. J. Virol. 91:e01795
    [Google Scholar]
  34. 34. 
    Lamp B, Url A, Seitz K, Eichhorn J, Riedel C et al. 2016. Construction and rescue of a molecular clone of deformed wing virus (DWV). PLOS ONE 11:e0164639
    [Google Scholar]
  35. 35. 
    Loope KJ, Baty JW, Lester PJ, Wilson Rankin EE 2019. Pathogen shifts in a honeybee predator following the arrival of the Varroa mite. Proc. R. Soc. B 286:20182499
    [Google Scholar]
  36. 36. 
    Mordecai GJ, Wilfert L, Martin SJ, Jones IM, Schroeder DC 2016. Diversity in a honey bee pathogen: first report of a third master variant of the Deformed Wing Virus quasispecies. ISME J 10:1264–73
    [Google Scholar]
  37. 37. 
    Mordecai GJ, Brettell L, Martin SJ, Dixon D, Jones IM, Schroeder DC 2016. Superinfection exclusion and the long-term survival of honey bees in Varroa-infested colonies. ISEM J 10:1182–91
    [Google Scholar]
  38. 38. 
    Fujiyuki T, Takeuchi H, Ono M, Ohka S, Sasaki T et al. 2004. RNA-like virus identified in the brains of aggressive worker honeybees. J. Virol. 78:1093–100
    [Google Scholar]
  39. 39. 
    Ongus JR, Peters D, Bonmatin JM, Bengsch E, Vlak JM, van Oers MM 2004. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol 85:3747–55
    [Google Scholar]
  40. 40. 
    Levin S, Sela N, Chejanovsky N 2016. Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor. Sci. Rep 6:37710
    [Google Scholar]
  41. 41. 
    Levin S, Sela N, Erez T, Nestel D, Pettis J et al. 2019. New viruses from the ectoparasite mite Varroa destructor infesting Apis mellifera and Apis cerana. Viruses 11:94
    [Google Scholar]
  42. 42. 
    Kevill JL, Highfield A, Mordecai GJ, Martin SJ, Schroeder DC 2017. ABC assay: method development and application to quantify the role of three DWV master variants in overwinter colony losses of European honey bees. Viruses 9:314
    [Google Scholar]
  43. 43. 
    Ryabov EV, Childers AK, Chen Y, Madella S, Nessa A, Evans JD 2017. Recent spread of Varroa destructor virus-1, a honey bee pathogen, in the United States. Sci. Rep. 7:17447
    [Google Scholar]
  44. 44. 
    McMahon DP, Natsopoulou ME, Doublet V, Furst M, Weging S et al. 2016. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. R. Soc. B 283:20160811
    [Google Scholar]
  45. 45. 
    Radzevičiūtė R, Theodorou P, Husemann M, Japoshvili G, Kirkitadze G et al. 2017. Replication of honey bee-associated RNA viruses across multiple bee species in apple orchards of Georgia, Germany and Kyrgyzstan. J. Invertebr. Pathol. 146:14–23
    [Google Scholar]
  46. 46. 
    De Souza FS, Kevill JL, Correia-Oliveira ME, de Carvalho CAL, Martin SJM 2019. Occurrence of deformed wing virus variants in the stingless Melipona subnitida and honey bee Apis mellifera populations in Brazil. Gen. J. Viol. 100:289–94
    [Google Scholar]
  47. 47. 
    Jamnikar-Ciglenecki U, Ocepek MP, Toplak I 2018. Genetic diversity of deformed wing virus from Apis mellifera carnica (Hymenoptera: Apidae) and varroa mite (Mesostigmata: Varroidae). J. Econ. Entomol. 312:11–19
    [Google Scholar]
  48. 48. 
    Moore J, Jironkin A, Chandler D, Burroughs N, Evans DJ et al. 2011. Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. J. Gen. Virol. 92:156–61
    [Google Scholar]
  49. 49. 
    Zioni N, Soroker V, Chejanovsky N 2011. Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1–deformed wing virus recombinant (VDV-1–DWV) in the head of the honey bee. Virology 417:106–12
    [Google Scholar]
  50. 50. 
    Wang H, Xie J, Shreeve TG, Ma J, Pallett DW et al. 2013. Sequence recombination and conservation of Varroa destructor virus-1 and Deformed wing virus in field collected honey bees (Apis mellifera). PLOS ONE 8:e74508
    [Google Scholar]
  51. 51. 
    Natsopoulou ME, McMahon DP, Doublet V, Frey E, Rosenkranz P, Paxton RJ 2017. The virulent, emerging genotype B of Deformed wing virus is closely linked to overwinter honeybee worker loss. Sci. Rep. 7:41045
    [Google Scholar]
  52. 52. 
    Cornman RS. 2017. Relative abundance of deformed wing virus, Varroa destructor virus 1, and their recombinants in honey bees (Apis mellifera) assessed by kmer analysis of public RNA-Seq data. J. Invertebr. Pathol. 149:44–50
    [Google Scholar]
  53. 53. 
    Dalmon A, Desbiez C, Coulon M, Thomasson M, Le Conte Y et al. 2017. Evidence for positive selection and recombination hotspots in Deformed wing virus (DWV). Sci. Rep. 7:41045
    [Google Scholar]
  54. 54. 
    Chejanovsky N, Ophir R, Schwager MS, Slabezki Y, Grossman S, Cox-Foster D 2014. Characterization of viral siRNA populations in honey bee colony collapse disorder. Virology 454:176–83
    [Google Scholar]
  55. 55. 
    Brettell LE, Martin SJ. 2017. Oldest Varroa tolerant honey bee population provides insight into the origins of the global decline of honey bees. Sci. Rep. 7:45953
    [Google Scholar]
  56. 56. 
    Annoscia D, Brown S, Di Prisco G, De Paoli G, Fabbro SD et al. 2018. 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. bioRxiv 257667. https://doi.org/10.1101/257667
    [Crossref]
  57. 57. 
    Zhang Y, Han R. 2018. A saliva protein of Varroa mites contributes to the toxicity toward Apis cerana and the DWV elevation in A. mellifera. Sci. Rep 8:3387
    [Google Scholar]
  58. 58. 
    Di Prisco G, Zhang X, Pennacchio F, Caprio E, Li J et al. 2011. Dynamics of persistent and acute deformed wing virus infections in honey bees (Apis mellifera). Viruses 3:2425–41
    [Google Scholar]
  59. 59. 
    DeGrandi-Hoffman G, Chen Y, Huang E, Huang MH 2010. The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). J. Insect Physiol. 56:1184–91
    [Google Scholar]
  60. 60. 
    Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E et al. 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. PNAS 110:18466–71
    [Google Scholar]
  61. 61. 
    Shah KS, Evans EC, Pizzorno MC 2009. Localization of deformed wing virus (DWV) in the brains of the honeybee, Apis mellifera Linnaeus. Virol. J 6:182
    [Google Scholar]
  62. 62. 
    Mockel N, Gisder S, Genersch E 2011. Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. J. Gen. Virol. 92:370–77
    [Google Scholar]
  63. 63. 
    Mazzei M, Carrozza ML, Luisi E, Forzan M, Giusti M et al. 2014. Infectivity of DWV associated to flower pollen: experimental evidence of a horizontal transmission route. PLOS ONE 9:e113448
    [Google Scholar]
  64. 64. 
    Gisder S, Möckel N, Eisenhardt D, Genersch E 2018. In vivo evolution of viral virulence: switching of deformed wing virus between hosts results in virulence changes and sequence shifts. Environ. Microbiol. 20:4612–28
    [Google Scholar]
  65. 65. 
    Yue C, Schröder M, Gisder S, Genersch E 2007. Vertical transmission routes for deformed wing virus of honeybees (Apis mellifera). J. Gen. Virol. 88:2329–36
    [Google Scholar]
  66. 66. 
    Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C et al. 2010. The German bee monitoring project: a long-term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–52
    [Google Scholar]
  67. 67. 
    Nordstrom S. 2003. Distribution of deformed wing virus within honey bee (Apis mellifera) brood cells infested with the ectoparasitic mite Varroa destructor. Exp. Appl. Acarol 29:293–302
    [Google Scholar]
  68. 68. 
    Kielmanowicz MG, Inberg A, Lerner IM, Golani Y, Brown N et al. 2015. Prospective large-scale field study generates predictive model identifying major contributors to colony losses. PLOS Pathog 11:e1004816
    [Google Scholar]
  69. 69. 
    Wu Y, Dong X, Kadowaki T 2017. Characterization of the copy number and variants of Deformed Wing Virus (DWV) in the pairs of honey bee pupa and infesting Varroa destructor or Tropilaelaps mercedesae. Front. Microbiol 8:1558
    [Google Scholar]
  70. 70. 
    Gisder S, Aumeier P, Genersch E 2009. Deformed wing virus: replication and viral load in mites (Varroa destructor). J. Gen. Virol. 90:463–67
    [Google Scholar]
  71. 71. 
    Campbell EM, Budge GE, Watkins M, Bowman AS 2016. Transcriptome analysis of the synganglion from the honey bee mite, Varroa destructor and RNAi knockdown of neural peptide targets. Insect Biochem. Mol. Biol. 70:116–26
    [Google Scholar]
  72. 72. 
    Santillán-Galicia MT, Ball BV, Clark SJ, Alderson PG 2010. Transmission of deformed wing virus and slow paralysis virus to adult bees (Apis mellifera L.) by Varroa destructor. J. Apic. Res 49:141–48
    [Google Scholar]
  73. 73. 
    Erban T, Harant K, Hubalek M, Vitamvas P, Kamler M et al. 2015. In-depth proteomic analysis of Varroa destructor: detection of DWV-complex, ABPV, VdMLV and honeybee proteins in the mite. Sci. Rep. 5:13907
    [Google Scholar]
  74. 74. 
    Martin SJ, Carreck NL, Ball BV 2013. The role of deformed wing virus in the initial collapse of varroa infested honey bee colonies in the UK. J. Apic. Res. 52:251–58
    [Google Scholar]
  75. 75. 
    Boncristiani HF, Di Prisco G, Pettis JS, Hamilton M, Chen YP 2009. Molecular approaches to the analysis of deformed wing virus replication and pathogenesis in the honey bee, Apis mellifera. Virol. J. 6:221
    [Google Scholar]
  76. 76. 
    Remnant EJ, Shi M, Buchmann G, Blacquière T, Holmes EC et al. 2017. A diverse range of novel RNA viruses in geographically distinct honey bee populations. J. Virol. 91:e00158–17
    [Google Scholar]
  77. 77. 
    de Miranda JR, Fries I 2008. Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J. Invertebr. Pathol. 98:184–89
    [Google Scholar]
  78. 78. 
    Amiri E, Kryger P, Meixner MD, Strand MK, Tarpy DR, Rueppell O 2018. Quantitative patterns of vertical transmission of deformed wing virus in honey bees. PLOS ONE 13:e0195283
    [Google Scholar]
  79. 79. 
    Amiri E, Meixner MD, Kryger P 2016. Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Sci. Rep. 6:33065
    [Google Scholar]
  80. 80. 
    Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N 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:e14357
    [Google Scholar]
  81. 81. 
    Ryabov EV. 2016. Invertebrate RNA virus diversity from a taxonomic point of view. J. Invertebr. Pathol. 147:37–50
    [Google Scholar]
  82. 82. 
    Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X et al. 2016. Redefining the invertebrate RNA virosphere. Nature 540:539–43
    [Google Scholar]
  83. 83. 
    Zhang X, He SY, Evans JD, Pettis JS, Yin GF, Chen YP 2012. New evidence that deformed wing virus and black queen cell virus are multi-host pathogens. J. Invertebr. Pathol. 109:156–59
    [Google Scholar]
  84. 84. 
    Genersch E, Yue C, Fries I, de Miranda JR 2006. Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J. Invertebr. Pathol. 91:61–63
    [Google Scholar]
  85. 85. 
    Levitt AL, Singh R, Cox-Foster DL, Rajotte E, Hoover K et al. 2013. Cross-species transmission of honey bee viruses in associated arthropods. Virus Res 176:232–40
    [Google Scholar]
  86. 86. 
    Tehel A, Brown MJ, Paxton RJ 2016. Impact of managed honey bee viruses on wild bees. Curr. Opin. Virol. 19:16–22
    [Google Scholar]
  87. 87. 
    Dolezal AG, Hendrix SD, Scavo NA, Carrillo-Tripp J, Harris MA et al. 2016. Honey bee viruses in wild bees: viral prevalence, loads, and experimental inoculation. PLOS ONE 11:e0166190
    [Google Scholar]
  88. 88. 
    Evison SEF, Roberts KE, Laurenson L, Pietravalle S, Hui J et al. 2012. Pervasiveness of parasites in pollinators. PLOS ONE 7:e30641
    [Google Scholar]
  89. 89. 
    McMahon DP, Wilfert L, Paxton RJ, Brown MJF 2018. Emerging viruses in bees: from molecules to ecology. Adv. Virus Res. 101:251–91
    [Google Scholar]
  90. 90. 
    Kojima Y, Toki T, Morimoto T, Yoshiyama M, Kimura K, Kadowaki T 2011. Infestation of Japanese native honey bees by tracheal mite and virus from non-native European honey bees in Japan. Microb. Ecol. 62:895–906
    [Google Scholar]
  91. 91. 
    Li J, Qin H, Wu J, Sadd BM, Wang X et al. 2012. The prevalence of parasites and pathogens in Asian honeybees Apis cerana in China. PLOS ONE 7:e47955
    [Google Scholar]
  92. 92. 
    Choe SE, Nguyen LTK, Noh JH, Koh HB, Jean YH et al. 2012. Prevalence and distribution of six bee viruses in Korean Apis cerana populations. J. Invertebr. Pathol. 109:330–33
    [Google Scholar]
  93. 93. 
    Martin SJ. 2001. The role of Varroa and viral pathogens in the collapse of honey bee colonies: a modelling approach. J. Appl. Ecol. 38:1082–93
    [Google Scholar]
  94. 94. 
    Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P 2011. Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. J. Appl. Environ. Microbiol. 78:981–87
    [Google Scholar]
  95. 95. 
    Benaets K, Van Geystelen A, Cardoen D, De Smet L, de Graaf DC et al. 2017. Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proc. R. Soc. B 284:20162149
    [Google Scholar]
  96. 96. 
    Remnant EJ, Mather N, Gillard TL, Yagound B, Beekman M 2019. Direct transmission by injection affects competition among RNA viruses in honeybees. Proc. R. Soc. B 286:20182452
    [Google Scholar]
  97. 97. 
    Tehel A, Vu Q, Bigot D, Gogol-Döring A, Koch P 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
    [Google Scholar]
  98. 98. 
    Khongphinitbunjong K, Neumann P, Chantawannakul P, Williams GR 2016. The ectoparasitic mite Tropilaelaps mercedesae reduces western honey bee, Apis mellifera, longevity and emergence weight, and promotes Deformed wing virus infections. J. Invertebr. Pathol. 137:38–42
    [Google Scholar]
  99. 99. 
    Sumpter D, Martin SJ. 2004. The dynamics of virus epidemics in Varroa-infested honeybee colonies. J. Anim. Ecol. 73:51–63
    [Google Scholar]
  100. 100. 
    Budge GE, Pietravalle S, Brown M, Laurenson L, Jones B et al. 2015. Pathogens as predictors of honey bee colony strength in England and Wales. PLOS ONE 10:e0133228
    [Google Scholar]
  101. 101. 
    Gauthier L, Ravallec M, Tournaire M, Cousserans F, Bergoin M et al. 2011. Viruses associated with ovarian degeneration in Apis mellifera L. queens. PLOS ONE 6:e16217
    [Google Scholar]
  102. 102. 
    Williams GR, Rogers RE, Kalkstein AL, Taylor BA, Shutler D, Ostiguy N 2009. Deformed wing virus in western honey bees (Apis mellifera) from Atlantic Canada and the first description of an overtly-infected emerging queen. J. Invertebr. Pathol. 101:77–79
    [Google Scholar]
  103. 103. 
    Calderone NW, Lin S, Kuenen LPS 2002. Differential infestation of honey bee Apis mellifera worker and queen brood by the parasitic mite Varroa destructor. Apidologie 33:389–98
    [Google Scholar]
  104. 104. 
    Dainat B, Neumann P. 2013. Clinical signs of deformed wing virus infection are predictive markers for honey bee colony losses. J. Invertebr. Pathol. 112:278–80
    [Google Scholar]
  105. 105. 
    Brettell LE, Mordecai GJ, Schroeder DC, Jones IM, da Silva JR et al. 2017. A comparison of deformed wing virus in deformed and asymptomatic honey bees. Insects 8:28
    [Google Scholar]
  106. 106. 
    Forsgren E, Fries I, de Miranda JR 2012. Adult honey bees (Apis mellifera) with deformed wings discovered in confirmed varroa-free colonies. J. Apic. Res. 51:136–38
    [Google Scholar]
  107. 107. 
    McMahon DP, Fürst MA, Caspar J, Theodorou P, Brown MJF, Paxton RJ 2015. A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J. Anim. Ecol. 84:615–24
    [Google Scholar]
  108. 108. 
    Martin SJ, Hardy J, Villalobos E, Martin-Hernandez R, Nikaido S, Higes M 2013. Do the honeybee pathogens Nosema ceranae and deformed wing virus act synergistically?. Environ. Microbiol. Rep. 5:506–10
    [Google Scholar]
  109. 109. 
    Costa C, Tanner G, Lodesani M, Maistrello L, Neumann P 2011. Negative correlation between Nosema ceranae spore loads and deformed wing virus infection levels in adult honey bee workers. J. Invertebr. Pathol. 108:224–25
    [Google Scholar]
  110. 110. 
    Doublet V, Natsopoulou ME, Zschiesche L, Paxton R 2015. Within-host competition among the honey bee pathogens Nosema ceranae and Deformed wing virus is asymmetric and to the disadvantage of the virus. J. Invertebr. Pathol. 124:31–34
    [Google Scholar]
  111. 111. 
    Zheng H-Q, Gong H-R, Huang S-K, Sohr A, Hu F-L, Chen YP 2015. Evidence of the synergistic interaction of honey bee pathogens Nosema ceranae and Deformed wing virus. Vet. Microbiol. 177:1–6
    [Google Scholar]
  112. 112. 
    Rortais A, Tentcheva D, Papachristoforou A, Gauthier L, Arnold G et al. 2006. Deformed wing virus is not related to honey bees’ aggressiveness. Virol. J. 3:61
    [Google Scholar]
  113. 113. 
    Baracchi D, Fadda A, Turillazzi S 2012. Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J. Insect Physiol. 58:1589–96
    [Google Scholar]
  114. 114. 
    Li J, Peng W, Wu J, Strange JP, Boncristiani H, Chen Y 2011. Cross-species infection of deformed wing virus poses a new threat to pollinator conservation. J. Econ. Entomol. 104:732–39
    [Google Scholar]
  115. 115. 
    Colla SR, Otterstatter MC, Gegear RJ, Thomson JD 2006. Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol. Conserve. 129:461–67
    [Google Scholar]
  116. 116. 
    Graystock P, Yates K, Evison SE, Darvill B, Goulson D, Hughes WO 2013. The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. J. Appl. Ecol. 50:1207–15
    [Google Scholar]
  117. 117. 
    Murray TE, Coffey MF, Kehoe E, Horgan FG 2013. Pathogen prevalence in commercially reared bumble bees and evidence of spillover in conspecific populations. Biol. Conserv. 159:269–76
    [Google Scholar]
  118. 118. 
    Eyer M, Chen YP, Schäfer MO, Pettis J, Neumann P 2009. Small hive beetle, Aethina tumida, as a potential biological vector of honeybee viruses. Apidologie 40:419–28
    [Google Scholar]
  119. 119. 
    Graystock P, Meeus I, Smagghe G, Goulson D, Hughes WO 2016. The effects of single and mixed infections of Apicystis bombi and deformed wing virus in Bombus terrestris. Parasitol 143:358–65
    [Google Scholar]
  120. 120. 
    Gisder S, Genersch E. 2017. Viruses of commercialized insect pollinators. J. Invertebr. Pathol. 147:51–59
    [Google Scholar]
  121. 121. 
    Manley R, Boots B, Wilfert L 2017. Condition-dependent virulence of slow bee paralysis virus in Bombus terrestris: Are the impacts of honeybee viruses in wild pollinators underestimated?. Oecologia 184:305–15
    [Google Scholar]
  122. 122. 
    Meeus I, de Miranda JR, de Graaf DC, Wäckers F, Smagghe G 2014. Effect of oral infection with Kashmir bee virus and Israeli acute paralysis virus on bumblebee (Bombus terrestris) reproductive success. J. Invertebr. Pathol. 121:64–69
    [Google Scholar]
  123. 123. 
    Hsu H-W, Chiu M-C, Shoemaker D, Yang C-CS 2018. Viral infections in fire ants lead to reduced foraging activity and dietary changes. Sci. Rep. 8:13498
    [Google Scholar]
  124. 124. 
    Carrillo-Tripp J, Dolezal AG, Goblirsch MJ, Miller WA, Toth AL et al. 2016. In vivo and in vitro infection dynamics of honey bee viruses. Sci. Rep. 6:22265
    [Google Scholar]
  125. 125. 
    McMenamin AJ, Flenniken ML. 2018. Recently identified bee viruses and their impact on three bee pollinators. Curr. Opin. Insect Sci. 26:120–29
    [Google Scholar]
  126. 126. 
    De Smet L, Ravoet J, de Miranda JR, Wenseleers T, Mueller MY et al. 2012. BeeDoctor, a versatile MLPA-based diagnostic tool for screening bee viruses. PLOS ONE 7:e47953
    [Google Scholar]
  127. 127. 
    Shumkova R, Neov B, Sirakova D, Georgieva A, Gadjev D et al. 2018. Molecular detection and phylogenetic assessment of six honeybee viruses in Apis mellifera L. colonies in Bulgaria. PeerJ 6:e5077
    [Google Scholar]
  128. 128. 
    Gajger IT, Kolodziejek J, Bakonyi T, Nowotny N 2014. Prevalence and distribution patterns of seven different honeybee viruses in diseased colonies: a case study from Croatia. Apidologie 45:701–6
    [Google Scholar]
  129. 129. 
    Mouret C, Lambert O, Piroux M, Beaudeau F, Provost B et al. 2013. Prevalence of 12 infectious agents in field colonies of 18 apiaries in western France. Revue Méd. Vét. 164:577–82
    [Google Scholar]
  130. 130. 
    Tencheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F et al. 2004. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol. 70:7185–91
    [Google Scholar]
  131. 131. 
    Pohorecka K, Bober A, Skubida M, Zdanska D 2011. Epizootic status of apiaries with massive losses of bee colonies (2008–2009). J. Apic. Sci. 55:137–48
    [Google Scholar]
  132. 132. 
    Simeunović P, Stevanović J, Vidanović D, Nišavić J, Radović D et al. 2014. A survey of deformed wing virus and acute bee paralysis virus in honey bee colonies from Serbia using real-time RT-PCR. Acta Vet 64:81–92
    [Google Scholar]
  133. 133. 
    Cirkovic D, Stevanovic J, Glavinic U, Aleksic N, Djuric S et al. 2018. Honey bee viruses in Serbian colonies of different strength. PeerJ 6:e5887
    [Google Scholar]
  134. 134. 
    Antúnez K, Anido M, Garrido-Bailón E, Botías C, Zunino P et al. 2012. Low prevalence of honeybee viruses in Spain during 2006 and 2007. Res. Vet. Sci. 93:1441–45
    [Google Scholar]
  135. 135. 
    Cepero A, Ravoet J, Gómez-Moracho T, Bernal J, Del Nozal M et al. 2014. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Res. Notes 7:649
    [Google Scholar]
  136. 136. 
    Buendía M, Martín-Hernández R, Ornosa C, Barrios L, Bartolomé C, Higes M 2018. Epidemiological study of honeybee pathogens in Europe: the results of Castilla-La Mancha (Spain). Span. J. Agric. Res. 16:e0502
    [Google Scholar]
  137. 137. 
    Berthoud H, Imdorf A, Haueter M, Radloff S, Neumann P 2010. Virus infections and winter losses of honey bee colonies (Apis mellifera). J. Apic. Res. 49:60–65
    [Google Scholar]
  138. 138. 
    Thompson CE, Biesmeijer JC, Allnutt TR, Pietravalle S, Budge GE 2014. Parasite pressures on feral honey bees (Apis mellifera sp.). PLOS ONE 9:e105164
    [Google Scholar]
  139. 139. 
    Ai H, Yan X, Han R 2012. Occurrence and prevalence of seven bee viruses in Apis mellifera and Apis cerana apiaries in China. J. Invertebr. Pathol. 109:160–64
    [Google Scholar]
  140. 140. 
    Yang B, Peng G, Li T, Kadowaki T 2013. Molecular and phylogenetic characterization of honey bee viruses, Nosema microsporidia, protozoan parasites, and parasitic mites in China. Ecol. Evol. 3:298–311
    [Google Scholar]
  141. 141. 
    Forsgren E, Wei S, Guiling D, Zhiguang L, Van Tran T et al. 2014. Preliminary observations on possible pathogen spill-over from Apis mellifera to Apis cerana. Apidologie 46:265–75
    [Google Scholar]
  142. 142. 
    Rodríguez M, Vargas M, Antúnez K, Gerding M, Ovídio CF, Zapata N 2014. Prevalence and phylogenetic analysis of honey bee viruses in the Biobío region of Chile and their association with other honey bee pathogens. Chil. J. Agric. Res. 74:170–77
    [Google Scholar]
  143. 143. 
    Guzman-Novoa E, Hamiduzzaman MM, Espinosa-Montaño LG, Correa-Benítez A, Anguiano-Baez R, Ponce-Vázquez R 2012. First detection of four viruses in honey bee (Apis mellifera) workers with and without deformed wings and Varroa destructor in Mexico. J. Apic. Res. 51:342–46
    [Google Scholar]
  144. 144. 
    Chen YP, Siede R. 2007. Honey bee viruses. Adv. Virus Res. 70:33–80
    [Google Scholar]
  145. 145. 
    Haddad N, Al-Gharaibeh M, Nasher A, Anaswah E, Alammari Y, Horth L 2018. Scientific note: molecular detection of pathogens in unhealthy colonies of Apis mellifera jemenitica. Apidologie 49:84–88
    [Google Scholar]
  146. 146. 
    Soroker V, Hetzroni A, Yakobson B, David D, David A et al. 2011. Evaluation of colony losses in Israel in relation to the incidence of pathogens and pests. Apidologie 42:192–99
    [Google Scholar]
  147. 147. 
    Loucif-Ayad W, Chefrour A, Algharibeh M, Haddad N 2013. First detection of Deformed wing virus of honeybees in Algeria. Phytoparasitica 41:445–47
    [Google Scholar]
  148. 148. 
    Ongus JR, Fombong AT, Irungu J, Masiga D, Raina S 2017. Prevalence of common honey bee pathogens at selected apiaries in Kenya, 2013–2014. Int. J. Trop. Insect Sci. 38:58–70
    [Google Scholar]
  149. 149. 
    Strauss U, Human H, Gauthier L, Crewe RM, Dietemann V, Pirk CWW 2013. Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata). J. Invertebr. Pathol. 114:45–52
    [Google Scholar]
  150. 150. 
    Abdi K, Belguith K, Hamdi C, Souissi Y, Essanaa J et al. 2018. Parasites-Iflavirus association and emergence of three master variants of DWV affecting Apis mellifera intermissa in Tunisian apiaries. Bull. Insectol. 71:273–82
    [Google Scholar]
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