Vertical-transmission routes for deformed wing virus of honeybees () Free

Abstract

Deformed wing virus (DWV) is a viral pathogen of the European honeybee (), associated with clinical symptoms and colony collapse when transmitted by the ectoparasitic mite . In the absence of , DWV infection does not result in visible symptoms, suggesting that mite-independent transmission results in covert infections. True covert infections are a known infection strategy for insect viruses, resulting in long-term persistence of the virus in the population. They are characterized by the absence of disease symptoms in the presence of the virus and by vertical transmission of the virus. To demonstrate vertical transmission and, hence, true covert infections for DWV, a detailed study was performed on the vertical-transmission routes of DWV. In total, 192 unfertilized eggs originating from eight virgin queens, and the same number of fertilized eggs from the same queens after artificial insemination with DWV-negative (three queens) or DWV-positive (five queens) semen, were analysed individually. The F0 queens and drones and F1 drones and workers were also analysed for viral RNA. By hybridization, viral sequences were detected in the ovary of an F0 queen that had laid DWV-positive unfertilized eggs and was inseminated with DWV-positive semen. In conclusion, vertical transmission of DWV from queens and drones to drone and worker offspring through unfertilized and fertilized eggs, respectively, was demonstrated. Viral sequences in fertilized eggs can originate from the queen, as well as from drones via DWV-positive semen.

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2007-08-01
2024-03-29
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References

  1. Bailey L., Ball B. V. 1991 Honey Bee Pathology , 2nd edn. London: Academic Press;
    [Google Scholar]
  2. Ball B. V., Allen M. F. 1988; The prevalence of pathogens in honey bee ( Apis mellifera ) colonies infested with the parasitic mite Varroa jacobsoni . Ann Appl Biol 113:237–244 [CrossRef]
    [Google Scholar]
  3. Berenyi O., Bakonyi T., Derakhshifar I., Köglberger H., Nowotny N. 2006; Occurence of six honeybee viruses in diseased Austrian apiaries. Appl Environ Microbiol 72:2414–2420 [CrossRef]
    [Google Scholar]
  4. Bergem M., Norberg K., Aamodt R. M. 2006; Long-term maintenance of in vitro cultured honeybee ( Apis mellifera ) embryonic cells. BMC Dev Biol 6:17 [CrossRef]
    [Google Scholar]
  5. Bowen-Walker P. L., Martin S. J., Gunn A. 1999; The transmission of deformed wing virus between honeybees ( Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J Invertebr Pathol 73:101–106 [CrossRef]
    [Google Scholar]
  6. Burden J. P., Griffiths C. M., Cory J. S., Smith P., Sait S. M. 2002; Vertical transmission of sublethal granulovirus infection in the Indian meal moth, Plodia interpunctuella . Mol Ecol 11:547–555 [CrossRef]
    [Google Scholar]
  7. Burden J. P., Nixon C. P., Hodgkinson A. E., Possee R. D., Sait S. M., King L. A., Hails R. S. 2003; Covert infections as a mechanism for long-term persistence of baculoviruses. Ecol Lett 6:524–531 [CrossRef]
    [Google Scholar]
  8. Chantawannakul P., Ward L., Boonham N., Brown M. 2006; A scientific note on the detection of honeybee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Tai honeybee ( Apis mellifera ) apiary. J Invertebr Pathol 91:69–73 [CrossRef]
    [Google Scholar]
  9. Chen Y. P., Pettis J. S., Feldlaufer M. F., Collins A. M., Smith I. B. 2004; Detection of deformed wing virus infection in honey bees, Apis mellifera L., in the United States. Am Bee J 144:557–559
    [Google Scholar]
  10. Chen Y. P., Higgins J. A., Feldlaufer M. F. 2005a; Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee ( Apis mellifera L.). Appl Environ Microbiol 71:436–441 [CrossRef]
    [Google Scholar]
  11. Chen Y., Pettis J. S., Feldlaufer M. F. 2005b; Detection of multiple viruses in queens of the honey bee Apis mellifera L. J Invertebr Pathol 90:118–121 [CrossRef]
    [Google Scholar]
  12. Chen Y., Evans J., Feldlaufer M. 2006a; Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera . J Invertebr Pathol 92:152–159 [CrossRef]
    [Google Scholar]
  13. Chen Y. P., Pettis J. S., Collins A., Feldlaufer M. F. 2006b; Prevalence and transmission of honeybee viruses. Appl Environ Microbiol 72:606–611 [CrossRef]
    [Google Scholar]
  14. Dimmock N. J., Primrose S. B. 1987 Introduction to Modern Virology Oxford: Blackwell Scientific;
    [Google Scholar]
  15. Fievet J., Tentcheva D., Gauthier L., De Miranda J. R., Cousserans F., Colin M. E., Bergoin M. 2006; Localization of deformed wing virus infection in queen and drone Apis mellifera L. Virol J 3:16 [CrossRef]
    [Google Scholar]
  16. Fries I., Camazine S. 2001; Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie 32:199–214 [CrossRef]
    [Google Scholar]
  17. Genersch E. 2005; Development of a rapid and sensitive RT-PCR method for the detection of deformed wing virus, a pathogen of the honeybee ( Apis mellifera ). Vet J 169:121–123 [CrossRef]
    [Google Scholar]
  18. Genersch E., Yue C., Fries I., de Miranda J. R. 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 [CrossRef]
    [Google Scholar]
  19. Heiles H. B. J., Genersch E., Kessler C., Neumann R., Eggers H. J. 1988; In situ hybridization with digoxigenin-labeled DNA of human papillomaviruses (HPV 16/18) in HeLa and SiHa cells. Biotechniques 6:978–981
    [Google Scholar]
  20. Kukan B. 1999; Vertical transmission of nucleopolyhedrosisvirus in insects. J Invertebr Pathol 74:103–111 [CrossRef]
    [Google Scholar]
  21. Lanzi G., De Miranda J. R., Boniotti M. B., Cameron C. E., Lavazza A., Capucci L., Camazine S. M., Rossi C. 2006; Molecular and biological characterization of deformed wing virus of honeybees ( Apis mellifera L.). J Virol 80:4998–5009 [CrossRef]
    [Google Scholar]
  22. Lipsitch M., Siller S., Nowak M. A. 1996; The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50:1729–1741 [CrossRef]
    [Google Scholar]
  23. Maori E., Tanne E., Sela I. 2007; Reciprocal sequence exchange between non-retro viruses and hosts leading to the appearance of new host phenotypes. Virology 362:342–349 [CrossRef]
    [Google Scholar]
  24. Martin S. J. 2001; The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J Appl Ecol 38:1082–1093
    [Google Scholar]
  25. Martin S., Hogarth A., Van Breda J., Perret J. 1998; A scientific note on Varroa jacobsoni Oudemans and the collapse of Apis mellifera L. colonies in the United Kingdom. Apidologie 29:369–370 [CrossRef]
    [Google Scholar]
  26. Mitta G., Vandenbulcke F., Noel T., Romestand B., Beauvillain J. C., Salzet M., Roch P. 2000; Differential distribution and defence involvement of antimicrobial peptides in mussel. J Cell Sci 113:2759–2769
    [Google Scholar]
  27. Nordström S., Fries I., Aarhus A., Hansen H., Korpela S. 1999; Virus infections in Nordic honey bee colonies with no, low or severe Varroa jacobsoni infestations. Apidologie 30:475–484 [CrossRef]
    [Google Scholar]
  28. Oldstone M. B. A. 2006; Viral persistence: parameters, mechanisms and future predictions. Virology 344:111–118 [CrossRef]
    [Google Scholar]
  29. Schley P. 1982; Neue Kolbenbesamungsspritze mit Sichtkontrolle und auswechselbaren Einsätzen. Allg Dtsch Imkerzeit 4:107–108 (in German
    [Google Scholar]
  30. Shen M., Yang X., Cox-Foster D., Cui L. 2005; The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 342:141–149 [CrossRef]
    [Google Scholar]
  31. Tentcheva D., Gauthier L., Zappulla N., Dainat B., Cousserans F., Colin M. E., Bergoin M. 2004; Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol 70:7185–7191 [CrossRef]
    [Google Scholar]
  32. Tentcheva D., Gauthier L., Bagny L., Fievet J., Dainat B., Cousserans F., Colin M. E., Bergoin M. 2006; Comparative analysis of deformed wing virus (DWV) RNA in Apis mellifera and Varroa destructor . Apidologie 37:41–50 [CrossRef]
    [Google Scholar]
  33. Yang X., Cox-Foster D. L. 2005; Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci U S A 102:7470–7475 [CrossRef]
    [Google Scholar]
  34. Yue C., Genersch E. 2005; RT-PCR analysis of Deformed wing virus in honey bees ( Apis mellifera ) and mites ( Varroa destructor ). J Gen Virol 86:3419–3424 [CrossRef]
    [Google Scholar]
  35. Yue C., Schröder M., Bienefeld K., Genersch E. 2006; Detection of viral sequences in semen of honeybees ( Apis mellifera ): evidence for vertical transmission of viruses through drones. J Invertebr Pathol 92:105–108 [CrossRef]
    [Google Scholar]
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