UDC 638.15:619:578

doi: 10.15389/agrobiology.2015.4.409eng

DEFORMED WING VIRUS IN Apis mellifera L.: PREVALENCE,
MORPHOLOGY, AND PATHOGENICITY (review)

V.E. Volykhina

IS.N. Vyshelesskii Institute of Experimental Veterinary, National Academy of Science of Belarus, 28, ul. Briketa, Minsk, 220003 the Republic of Belarus,
e-mail Volykhina@rambler.ru

Received November 25, 2014


Viral infections are not considered the most dangerous honeybee (Apis mellifera L.) diseases though being rather harmful. Virus-caused honeybee pathologies are mainly symptomless (N.J. Dimmock et al., 1987; A.C.F. Hung et al., 1996), nevertheless, a rapid replication of the viruses can be triggered leading to clinical manifestation and even death of the insects (R. Singh et al., 2010). In honeybee families a simultaneous circulation of several viruses can occur. Acute bee paralysis virus (ABPV), deformed wing virus (DWV) in Europe, and Kashmir bee virus (KBV), Israeli acute bee paralysis virus (IABPV) and DWV in the United States seem to be related to honeybee family collapse. This review summarizes the data about one of the most prevalent honeybeeviruses, DWV (D. Tentcheva et al., 2004; O. Berènyi et al., 2006; S.L. Nielsen et al., 2008; S. Ruba et al., 2012). Surveys showed DWV in European countries. In Austria, France and Denmark the DWV was found in 91, 97 and 57 % of the apiaries surveyed; in the Czech Republic 31 % of sampled bees were infected with DWV (note, other viruses in Austria and France were less frequent, i.e. 68 and 58 %, respectively, for ABPV; 49 и 86 % for sacbrood virus, SBV; 30 and 86 % for black queen cell virus, BQCV; and 10 and 28 % for chronic bee paralysis virus, CBРV) (D. Tentcheva et al., 2004; O. Berényi et al., 2006). DWV predominated in the apiaries of all studied regions of Russia (A. Kalashnikov et al., 2012), and in Moscow Province only DWV and SBV were revealed. DWV is detected in Apis florea and A. dorsata (X. Zhang et al., 2012). Free DWV dissemination was indicated among some insects other than Apis (Bombus terrestris, B. pascuorum, B. huntii Green) (E. Genersch et al., 2005; J. Li et al., 2011; A.L. Levitt et al., 2013). DWV, a RNA virus with monocistronic genome, is a member of the genus Iflavirus (Iflaviridae family, Picornavirales) (G. Lanzi et al., 2006). Its phylogenetic relationship with Kakugo virus (T. Fujiyuki et al., 2004; A. Rortais et al., 2006) has been confirmed. The identity of the RNA nucleotide sequences of virus isolates from different geographic locations is 98-99 % (O. Berènyi et al., 2007). Its structural proteins VP1-3 are similar to the corresponding picornavirus structural proteins, while a low molecular weight protein VP4 is not found (G. Lanzi et al., 2006). The main targets of deformed wing virus are reproductive organs and digestive tract of bees (Y.P. Chen et al., 2006; J. Fievet et al., 2006). The viral RNA is also found in the wings, head, thorax, hemolymph, fat body (J. Fievet et al., 2006; H.F. Boncristiani et al., 2009). It can be detected during all life stages of honeybee (Y.P. Chen et al., 2005). The brood and adults with clinical manifestations of the disease die (L. Bailey et al., 2010). The worker bees are most sensitive to DWV. The bee colonies are weakened; they are characterized by reduced size and prone to sudden collapse (G. Lanzi et al., 2006; R.M. Johnson et al., 2009). The peak incidence is in the autumn. In addition to vector transmission a horizontal per os and also a vertical transovarial transmission of the virus are possible (C. Yue et al., 2005; C. Yue et al., 2007). The virus can cause a latent infection without visible symptoms of the disease with prolonged persistence of the pathogen in the host and vertical virus transmission or subclinical shorter form with high rate of viral replication and more pathogenic horizontal transmission. For clinical outbreak of DWV infection followed by colony collapse a strong trigger is required, such as immunosuppression by mites Varroa destructor or V. destructor as biological vector. The apiaries with V. destructor infestation are often infected by DWV.

Keywords: deformed wing virus, honeybee Apis mellifera L., bee family, collapse, virus transmission by vectors, per os transmission, vertical transovarial transmission.

 

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REFERENCES

  1. Schroeder D.C., Martin S.J. Deformed wing virus. The main suspect in unexplained honeybee deaths worldwide. Virulence, 2012, 3(7): 589-591.
  2. Chen Y.P., Siede R. Honey bee viruses. Adv. Virus Res., 2007, 70: 33-80 CrossRef
  3. Bailey L., Carpenter J.M., Woods R.D. Properties of a filamentous virus of the honey bee (Apis mellifera). Virology, 1981, 114(1): 1-7 CrossRef
  4. Tokarz R., Firth C., Street C., Cox-Foster D.L. Lack of evidence for an association between Iridovirus and colony collapse disorder. PLoS ONE, 2011, 6(6): e21844 CrossRef
  5. Olivier V., Blanchard P., Chaouch S., Lallemand P., Schurr F., Cel-
    le O., Dubois E., Tordo N., Thiéry R., Houlgatte R., Ribière M. Molecular characterisation and phylogenetic analysis of Chronic bee paralysis virus, a honey bee virus. Virus Res., 2008, 132(1-2): 59-68 CrossRef
  6. Singh R., Levitt A.L., Rajotte E.G., Holmes E.C., Ostiguy N., van Engelsdorp D., Lipkin W.I., de Pamphilis C.W., Toth A.L., Cox-Fos-
    ter D. RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE, 2010, 5(12): e14357 CrossRef
  7. Dimmock N.J., Primrose S.B.  Introduction to modern virology. Primrose, 1987.
  8. Hung A.C.F., Shimanuki H., Knox D.A. Inapparent infection of acute bee paralysis virus and Kashmir bee virus in the U.S. honey bees. American Bee Journal, 1996, 136: 874-876.
  9. Rortais A., Tentcheva D., Papachristoforou A., Gauthier L., Arnold G., Colin M., Bergoin M. Deformed wing virus is not related to honey bees' aggressiveness. Virol. J., 2006, 3: 61 CrossRef
  10. Bailey L., Ball B.V.Honey bee pathology. 2nd ed. Academic Press, London, 1991.
  11. Lanzi G., de Miranda J.R., Boniotti M.B., Cameron C.E., Lavazza A., Capucci L., Camazine S.M., Rossi C. Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). J. Virol., 2006, 80(10): 4998-5009 CrossRef
  12. Baker A.C., Schroeder D.C. The use of RNA-dependent RNA polymerase for the taxonomic assignment of Picorna-like viruses (order Picrornavirales) infecting Apis mellifera L. populations. Virol. J., 2008, 5: 10 CrossRef
  13. Tentcheva D., Gauthier L., Zappulla N., Dainat B., Cousserans F., Colin M.E., Bergoin M. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol., 2004, 70(12): 7185-7191 CrossRef
  14. Berényi O., Bakonyi T., Derakhshifar I., Koglberger H., Nowothy N. Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl. Environ. Microbiol., 2006, 72(4): 2414-2420.
  15. Nielsen S.L., Nicolaisen M., Kryger P. Incidence of acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus, deformed wing virus, Kashmir bee virus and sacbrood virus in honey bees (Apis mellifera) in Denmark. Apidologie, 2008, 39: 310-314 CrossRef
  16. Ryba S., Titera D., Schodelbauerova-Traxmandlova I., Kindlmann P. Prevalence of honeybee viruses in the Czech Republic and coinfections with other honeybee disease. Biologia, 2012, 67(3): 590-595 CrossRef
  17. Kalashnikov A.E., Udina I.G. Rasprostranenie RNK-soderzhashchikh virusov u pchely medonosnoi Apis mellifera L. na territorii Rossii. FarmAnimals, 2012, 1: 72-76.
  18. Zhang X., He S.Y., Evans J.D., Pettis J.S., Yin G.F., Chen Y.P. New evidence that deformed wing virus and black queen cell virus are multi-host pathogens. J. Invert. Pathol., 2012, 109(1): 156-159 CrossRef
  19. Genersch E., Yue C., Fries I., de Miranda J.R. Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J. Invert. Pathol., 2006, 91(1): 61-63 CrossRef
  20. Li J., Peng W., Wu J., Strange J.P., Boncristiani H., Chen Y. Cross-species infection of deformed wing virus poses a new threat to pollinator conservation. J. Econom. Entomol., 2011, 104(3): 732-739 CrossRef
  21. Levitt A.L., Singh R., Cox-Foster D.L., Rajotte E., Hoover K., Osti-
    guy N., Holmes E.C. Cross-species transmission of honey bee viruses in associated arthropods. Virus Res., 2013, 176(1-2): 232-240 CrossRef
  22. Dimmork N.J., Easton A.J., Leppard K.N. Introduction to modern virology. 6th ed. Blackwell Publishing, Malden, 2007.
  23. Straier L. Biokhimiya. Tom 3 [Biochemistry. V. 3]. Moscow, 1985.
  24. Berenyi O., Bakonyi T., Derakhshifar I., Koglberger H., Topolska G., Ritter W. Phylogenetic analysis of deformed wing virus genotypes from diverse geographic origins indicates recent global distribution of the virus. Appl. Environ. Microbiol., 2007, 73(11): 3605-3611 CrossRef
  25. Liljas L., Tate J., Lin P., Christian P., Johnson J.E. Evolutionary and taxonomic implications of conserved structural motifs between picornaviruses and insect picorna-like viruses. Arch. Virol., 2002, 147: 59-84 CrossRef
  26. Chen Y.P., Pettis J.S., Collins A., Feldlaufer M.F. Prevalence and transmission of honeybee viruses. Appl. Environ. Microbiol., 2006, 72(1): 606-611 CrossRef
  27. Fievet J., Tentcheva D., Gauthier L., De Miranda J.R., Cousserans F., Colin M.E., Bergoin M. Localization of deformed wing virus infection in queen and drone Apis mellifera L. Virol. J., 2006, 3: 16 CrossRef
  28. Ongus J.R., Peters D., Bonmatin J.M., Bengsch E., Vlak J.M., vanOers M.M. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol., 2004, 85: 3747-3755 CrossRef
  29. Fujiyuki T., Takeuchi H., Ono M., Ohka S., Sasaki T., Nomoto A., Ku-
    bo T. Novel insect picorna-like virus identified in the brains of aggressive worker honeybees. J. Virol., 2004, 78: 1093-1100 CrossRef
  30. Wang H., Xie J., Shreeve T.G., Ma J., Pallett D.W., King L.A., Possee R.D. Sequence recombination and conservation of Varroa destructor Virus-1 and Deformed Wing Virus in field collected honey bees (Apis mellifera). PloS ONE, 2013, 8(9): e74508 CrossRef
  31. Boncristiani H.F., Di Prisco G., Pettis J.S., Hamilton M., Chen Y.P. Molecular approaches to the analysis of deformed wing virus replication and pathogenesis in the honey bee, Apis mellifera. Virol. J., 2009, 11(6): 221 CrossRef
  32. Fusa J.R., Richter A.R. Virulence and multigeneration passage of a nuclear polyhedrosis virus selected for an increased rate of vertical transmission. Biol. Control, 1992, 2: 171-175.
  33. Shah K.S, Evans E.C., Pizzorno M.C. Localization of deformed wing virus in the brains of the honeybee, Apis mellifera Linnaeus. Virol. J., 2009, 30(6): 182 CrossRef
  34. Yang X., Cox-Foster D. Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. PNAS USA, 2005, 102(21): 7470-7475 CrossRef
  35. Engels W. Occurrence and significance of vitellogenins in female castes of social Hymenoptera. Amer. Zool., 1974, 14: 1229-1237.
  36. Chen Y.P., Higgins J.A., Feldlaufer M.F. Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Appl. Environ. Microbiol., 2005, 71(1): 436-441 CrossRef
  37. De Miranda J.R., Genersch E. Deformed wing virus. J. Invert. Pathol., 2010, 103(Suppl. 1): 48-61.
  38. Kovac H., Crailsheim K. Lifespan of Apis mellifera carnica Pollm infested by Varroa jacobsoni in relation to season and extent of infestation. Journal of Apicultural Research, 1988, 27: 230-238.
  39. Johnson R.M., Evans J.D., Robinson G.E., Berenbaum M.R. Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). PNAS USA, 2009, 35(106): 14790-14795 CrossRef
  40. Dainat B., Evans J.D., Chen Y.P., Gauthier L., Neumann P. Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl. Environ. Microbiol., 2013, 78(4): 981-987 CrossRef
  41. Iqbal J., Mueller U. Virus infection causes specific learning deficits in honeybee foragers. Proc. Biol. Sci., 2007, 274(1617): 1517-1521 CrossRef
  42. Navajas M., Migeon A., Alaux C., Martin-Magniett M., Robinson G., Evans J., Cros-Arteil S., Crauser D., Le Conte Y. Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics, 2008, 9: 301 CrossRef
  43. Terio V., Martella V., Camero M., Decado N., Testini G., Bonerba E., Tantillo G. Detection of a honeybee iflavirus with intermediate characteristics between kakugo virus and deformed wing virus. New Microbiology, 2008, 31(4): 439-444.
  44. Engelhard E.K. The insect tracheal system: A conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. PNAS USA, 1994, 91: 3224-3227 CrossRef
  45. Ball B.V., Allen M.F. The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Ann. Appl. Biol., 1988, 113: 237-244 CrossRef
  46. Shimanuki H., Calderone N.W., Knox D.A. Parasitic mite syndrome: the symptoms. American Bee Journal, 1994, 134: 827-828.
  47. Nordström S. Virus infection in Nordic honeybee colonies with no, low or severe Varroa jacobsoni infestations. Apidologie, 1999, 30: 475-484.
  48. Yang X., Cox-Foster D. Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology, 2007, 134(Pt 3): 405-412 CrossRef
  49. Prisco G.D., Zhang X., Pennacchio F., Caprio E., Li J., Evans J.D., Degrandi-Hoffman G., Hamilton M., Chen Y.P. Dynamic of persistent and acute deformed wing virus infection in honey bees, Apis mellifera. Viruses, 2011, 3(12): 2425-2441 CrossRef
  50. Yue C., Genersch E. RT-PCR analysis of Deformed wing virus in honey bees (Apis mellifera) and mites (Varroa destructor). J. Gen. Virol., 2005, 86(Pt 12): 3419-3424.
  51. Bowen-Walker P.L., Martin S.J., Gunn A. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite varroa jacobsoni. J. Invert. Pathol., 1999, 73(1): 101-106.
  52. Tentcheva D., Gauthier L., Jouve S., Canabady-Rochelle L., Dainat B., Cousserans F., Colin M.E., Ball B.V., Bergoin M. Polymerase chain reaction detection of deformed wing virus (DWV) in Apis mellifera L. and Varroa destructor. Apidologie, 2004, 35: 431-439 CrossRef
  53. Bakonyi T., Farkas R., Szendroi A., Dobos-Kovács M., Rusvai M. Detection of acute bee paralysis virus by RT-PCR in honey bee and Varroa destructor field samples: rapid screening of representative Hungarian apiaries. Apidologie, 2002, 33: 63-74 CrossRef
  54. Zhang Q., Ongus J.R., Boot W.J., Calis J., Bonmatin J.M., Bengsch E. Detection and localization of picorna-like virus particles in tissues of Varroa destructor, an ectoparasite of the honey bee, Apis mellifera. J. Invert. Pathol., 2007, 96(2): 97-105.
  55. Santillán-Galicia M.T., Carzaniga R., Ball B.V., Alderson P.G. Immunolocalization of deformed wing virus particles within the mite Varroa destructor. J. Gen. Virol., 2008, 89(Pt 7): 1685-1689.
  56. Gisder S., Aumeier P., Genersh E. Deformed wing virus: replication and viral load in mites (Varroa destructor). J. Gen. Virol., 2009, 90(2): 463-467 CrossRef
  57. Dall D.J. Inapparent infection of honey bee pupae by Kashmir and sacbrood bee viruses in Australia. Ann. Appl. Biol., 1985, 106: 461-468 (doi: 10.1111/j.1744-7348.1985.tb03136.x).
  58. Bailey L., Ball B.V., Perry J.N. Association of viruses with two protozoal pathogens of the honey bee. Ann. Appl. Biol., 1983, 103: 13-20 CrossRef
  59. Charvet R., Katouzian-Safadi M., Colin M.E., Marchard P.A., Bon-matin J.M. Systemic insecticides: new risk for pollinator insects. Annals of Pharmacology Fr., 2004, 62(1): 29-35.
  60. Colin M.E., Bonmatin J.M., Moineau I., Gaimon C., Brun S., Vermandere J.P. A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Arch. Environ. Con. Tox., 2004, 47(3): 387-395 CrossRef
  61. Genersch E., Aubert M. Emerging and re-emerging viruses of the honey bee (Apis mellifera L). Veterinary Research, 2010, 41(6): 54 CrossRef
  62. Schöning C., Gisder S., Geiselhardt S., Kretschmann I., Bienefeld K., Hilker M., Genersh E. Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera. J. Exp. Biol., 2012, 215(Pt 2): 264-271.
  63. Parker P., Guarna M.M., Melathopoulos A.P., Kyung-Mee Moon, White R., Huxter E., Pernal S.F., Foster L.J. Correlation of proteome-wide changes with social immunity behaviors provides insight into resistance to the parasitic mite, Varroa destructor, in the honey bee (Apis mellifera). Genome Biology, 2012, 13(9): R. 81 CrossRef
  64. Richard F.J., Holt H.L., Grozinger C.M. Effects of immunostimulation on social behavior, chemical communication and genome-wide gene expression in honey bee workers (Apis mellifera). BMC Genomics, 2012, 13: 558 CrossRef
  65. McDonnell C.M., Alaux C., Parrinello H., Desvignes J.P., Crauser D., Durbesson E., Beslay D. Ecto- and endoparasite induce similar chemical and brain neurogenomic responses in the honey bee (Apis mellifera). BMC Ecology, 2013, 13(1): 25 CrossRef
  66. Weinberg K.P., Madel G. The influence of the mite Varroa jacobsoni on the protein concentration and the haemolymph volume of the blood of the worker bees and drones of the honey bee Apis mellifera. Apidologie, 1985, 16: 421-436.
  67. Daly H.V., DeJong D., Stone N.D. Effect of parasitism by Varroa jacobsoni on morphometrics of Africanized worker honey-bees. Journal of Apicultural Research, 1988, 27: 126-130.
  68. Koch W., Ritter W. Experimental examinations concerning the problem of deformed emerging bees after infestation with Varroa jacobsoni. J. Vet. Med., 1991, 38: 337-344.
  69. Marcangeli J., Monetti L., Fernandez N. Malformations produced by Varroa jacobsoni on Apis mellifera in the province of Buenos Aires, Argentina. Apidologie, 1992, 23: 399-402.
  70. Nordström S. Distribution of deformed wing virus within honey bee (Apis mellifera) brood cells infested with the ectoparasitic mite Varroa destructor. Exp. Appl. Acarol., 2003, 29: 293-302.
  71. Nordström S. Virus infections and varroa mite infestations in honey bee colonies. PhD thesis. Swedish University of Agricultural Sciences, Sweden, 2000.
  72. Chen Y.P., Smith I.B., Collins A.M.,Pettis J.S., Feldlaufer M.F. Detection of deformed wing virus infection in honey bees, Apis mellifera L., in the United States. American Bee Journal, 2004, 144: 557-559.
  73. Highfield A.C., Nagar A.E., Mackinder L.C., Noël L.M., Hall M.J., Martin S.J., Schroeder D.C. Deformed wing virus implicated in overwintering honeybee colony losses. Appl. Environ. Microbiol., 2009, 75(22): 7212-7220 CrossRef
  74. Chen Y.P., Pettis J.S., Feldlaufer M.F. Detection of multiple viruses in queens of the honey bee Apis mellifera L. J. Invert. Pathol., 2005, 90: 118-121 CrossRef
  75. De Miranda J.R., Fries I. Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J. Invert. Pathol., 2008, 98(2): 184-189 (doi: 10.1016/j.jip.2008.02.004).
  76. Yue C., Schröder M., Gisder S., Genersch E. Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). J. Gen. Virol., 2007, 88(Pt 8): 2329-2336 CrossRef
  77. Yue C., Schröder M., Bienefeld K., Genersch E. Detection of viral sequences in semen of honeybees (Apis mellifera): evidence for vertical transmission of viruses through drones. J. Invert. Pathol., 2006, 92: 105-108 CrossRef
  78. Calderón R.A., van Veen J.W., Sommeijer M.J., Sanchez L.A. Reproductive biology of Varroa destructor in Africanized honey bees (Apis mellifera). Exp. Appl. Acarol., 2010, 50(4): 281-297 CrossRef

 

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