1887

Abstract

Recent reports on a steady decline of honeybee colonies in several parts of the world caused great concern. There is a consensus that pathogens are among the key players in this alarming demise of the most important commercial pollinator. One of the pathogens heavily implicated in colony losses is deformed wing virus (DWV). Overt DWV infections manifested as deformed-wing syndrome started to become a threat to honeybees only in the wake of the ectoparasitic mite , which horizontally transmits DWV. However, a direct causal link between the virus and the symptom ‘wing deformity’ has not been established yet. To evaluate the impact of different horizontal transmission routes, and especially the role of the mite in the development of overt DWV infections, we performed laboratory infection assays with pupae and adult bees. We could demonstrate that pupae injected with DWV dose-dependently developed overt infections characterized by deformed wings in adult bees, suggesting that DWV, if transmitted to pupae by the mite, is the causative agent of the deformed-wing syndrome. The OID (overt infection dosage) was approximately 2500 genome equivalents. Injecting more than 1×10 DWV genome equivalents into adult bees also resulted in overt infections while the same viral dosage fed to adult bees only resulted in covert infections. Therefore, both infection of adult bees through DWV-transmitting phoretic mites and infection of nurse bees through their cannibalizing DWV-infected pupae might represent possible horizontal transmission routes of DWV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.025940-0
2011-02-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/2/370.html?itemId=/content/journal/jgv/10.1099/vir.0.025940-0&mimeType=html&fmt=ahah

References

  1. Amann, R. I., Binder, B. J., Olson, R. J., Chisholm, S. W., Devereux, R. & Stahl, D. A.(1990). Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56, 1919–1925. [Google Scholar]
  2. Ball, B. V.(1989).Varroa jacobsoni as a virus vector. In Present Status of Varroatosis in Europe and Progress in the Varroa Mite Control, pp. 241–244. Edited by Cavalloro, R.. Luxembourg. : Office for Official Publications of the European Communities. [Google Scholar]
  3. Ball, B. V. & Allen, M. E.(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]
  4. Bonsall, M. B., Sait, S. M. & Hails, R. S.(2005). Invasion and dynamics of covert infection strategies in structured insect-pathogen populations. J Anim Ecol 74, 464–474.[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., 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]
  7. Chen, Y. P., Higgins, J. A. & Feldlaufer, M. F.(2005). 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]
  8. Chen, Y. P., Pettis, J. S., Collins, A. & Feldlaufer, M. F.(2006). Prevalence and transmission of honeybee viruses. Appl Environ Microbiol 72, 606–611.[CrossRef] [Google Scholar]
  9. Cox-Foster, D. L., Conlan, S., Holmes, E. C., Palacios, G., Evans, J. D., Moran, N. A., Quan, P.-L., Briese, S., Hornig, M. & other authors(2007). A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318, 283–287.[CrossRef] [Google Scholar]
  10. de Miranda, J. R. & Fries, I.(2008). Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J Invertebr Pathol 98, 184–189.[CrossRef] [Google Scholar]
  11. de Miranda, J. R. & Genersch, E.(2010). Deformed wing virus. J Invertebr Pathol 103, S48–S61.[CrossRef] [Google Scholar]
  12. Evans, J. D. & Spivak, M.(2010). Socialized medicine: individual and communal disease barriers in honey bees. J Invertebr Pathol 103, S62–S72.[CrossRef] [Google Scholar]
  13. Ewald, P. W.(1983). Host–parasite relations, vectors, and the evolution of disease severity. Annu Rev Ecol Syst 14, 465–485.[CrossRef] [Google Scholar]
  14. Ewald, P. W. & De Leo, G.(2002). Alternative transmission modes and the evolution of virulence. In Adaptive Dynamics of Infectious Diseases: in Pursuit of Virulence Management, pp. 10–25. Edited by Dieckmann, U., Metz, J. A. J., Sabelis, M. W. & Sigmund, K.. Cambridge, UK. : Cambridge University Press. [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.(1993).Nosema apis – a parasite in the honey bee colony. Bee World 74, 5–19.[CrossRef] [Google Scholar]
  17. Fries, I.(2010).Nosema ceranae in European honey bees (Apis mellifera). J Invertebr Pathol 103, S73–S79.[CrossRef] [Google Scholar]
  18. Fries, I. & Camazine, S.(2001). Implications of horizontal and vertical pathogen transmission for honeybee epidemiology. Apidologie (Celle) 32, 199–214.[CrossRef] [Google Scholar]
  19. 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]
  20. Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Büchler, R., Berg, S., Ritter, W., Mühlen, W. & other authors(2010). The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41, 332–352.[CrossRef] [Google Scholar]
  21. Gisder, S., Aumeier, P. & Genersch, E.(2009). Deformed wing virus (DWV): viral load and replication in mites (Varroa destructor). J Gen Virol 90, 463–467.[CrossRef] [Google Scholar]
  22. Guzmán-Novoa, E., Eccles, L., Calvete, Y., Mcgowan, J., Kelly, P. G. & Correa-Benítez, A.(2010).Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie 41, 443–450.[CrossRef] [Google Scholar]
  23. Hails, R. S., Ball, B. V. & Genersch, E.(2008). Infection strategies of insect viruses. In Virology and the Honey Bee, pp. 255–275. Edited by Aubert, M., Ball, B. V., Fries, I., Moritz, R. F. A., Milani, N. & Bernardinelli, I.. Luxembourg. : European Communities. [Google Scholar]
  24. Highfield, A. C., El Nagar, A., Mackinder, L. C. M., Noël, L. M.-L. J., Hall, M. J., Martin, S. J. & Schroeder, D. C.(2009). Deformed wing virus implicated in over-wintering honeybee colony losses. Appl Environ Microbiol 75, 7212–7220.[CrossRef] [Google Scholar]
  25. Iqbal, J. & Mueller, U.(2007). Virus infection causes specific learning deficits in honeybee foragers. Proc Biol Sci 274, 1517–1521.[CrossRef] [Google Scholar]
  26. 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]
  27. 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]
  28. Martin, S. J., Hogarth, A., van Breda, J. & Perrett, J.(1998). A scientific note on Varroa jacobsoni Oudemans and the collapse of Apis mellifera colonies in the United Kingdom. Apidologie 29, 369–370.[CrossRef] [Google Scholar]
  29. Ratnieks, F. L. W. & Carreck, N. L.(2010). Clarity on honey bee collapse? Science 327, 152–153.[CrossRef] [Google Scholar]
  30. Ribiere, M.(2006) Infectious chronic bee paralysis virus (CBPV) excretion in honey bee (Apis mellifera L.) feces: A way of spread. Proceedings of the 2nd EurBee Conference, Prague 2006.
  31. Santillán-Galicia, M. T., Ball, B. V., Clark, S. J. & Alderson, P. G.(2010). Transmission of deformed wing virus and slow paralysis virus to adult bees (Apis mellifera L.) by Varroa destructor.J Apic Res 49, 141–148.[CrossRef] [Google Scholar]
  32. Shah, K. S., Evans, E. C. & Pizzorno, M. C.(2009). Localization of deformed wing virus (DWV) in the brains of the honeybee, Apis mellifera Linnaeus. Virol J 6, 182.[CrossRef] [Google Scholar]
  33. Siede, R., König, M., Büchler, R., Failing, K. & Thiel, H. J.(2008). A real-time PCR based survey on acute bee paralysis virus in German bee colonies. Apidologie 39, 650–661.[CrossRef] [Google Scholar]
  34. 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]
  35. vanEngelsdorp, D.(2008). A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS ONE 3, e4071.[CrossRef] [Google Scholar]
  36. vanEngelsdorp, D. & Meixner, M. D.(2010). A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invertebr Pathol 103, S80–S95.[CrossRef] [Google Scholar]
  37. vanEngelsdorp, D., Evans, J. D., Saegerman, C., Mullin, C., Haubruge, E., Nguyen, B. K., Frazier, M., Frazier, J., Cox-Foster, D. & other authors(2009). Colony collapse disorder: a descriptive study. PLoS ONE 4, e6481.[CrossRef] [Google Scholar]
  38. 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]
  39. Yue, C. & Genersch, E.(2005). RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J Gen Virol 86, 3419–3424.[CrossRef] [Google Scholar]
  40. Yue, C., Schröder, M., Gisder, S. & Genersch, E.(2007). Vertical transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol 88, 2329–2336.[CrossRef] [Google Scholar]
  41. Yue, D., Nordhoff, M., Wieler, L. H. & Genersch, E.(2008). Fluorescence in situ-hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environ Microbiol 10, 1612–1620.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.025940-0
Loading
/content/journal/jgv/10.1099/vir.0.025940-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error