Honey Bee Queens and Virus Infections
Abstract
:1. Introduction
2. Viral Transmission Modes to Honey Bee Queens
3. Direct Health Impacts of Viruses on Queens
4. Case Study of IAPV Effects on Queen Attractiveness and Immune Priming
5. Discussion
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Moritz, R.F.A.; de Miranda, J.; Fries, I.; Le Conte, Y.; Neumann, P.; Paxton, R.J. Research strategies to improve honeybee health in Europe. Apidologie 2010, 41, 227–242. [Google Scholar] [CrossRef] [Green Version]
- Vanengelsdorp, D.; Evans, J.D.; Saegerman, C.; Mullin, C.; Haubruge, E.; Nguyen, B.K.; Frazier, M.; Frazier, J.; Cox-Foster, D.; Chen, Y.; et al. Colony collapse disorder: A descriptive study. PLoS ONE 2009, 4, e6481. [Google Scholar] [CrossRef] [PubMed]
- vanEngelsdorp, D.; Meixner, M.D. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol. 2010, 103, S80–S95. [Google Scholar] [CrossRef] [PubMed]
- Smith, K.M.; Loh, E.H.; Rostal, M.K.; Zambrana-Torrelio, C.M.; Mendiola, L.; Daszak, P. Pathogens, pests, and economics: Drivers of honey bee colony declines and losses. EcoHealth 2013, 10, 434–445. [Google Scholar] [CrossRef] [PubMed]
- Steinhauer, N.; Kulhanek, K.; Antúnez, K.; Human, H.; Chantawannakul, P.; Chauzat, M.-P.; vanEngelsdorp, D. Drivers of colony losses. Curr. Opin. Insect Sci. 2018, 26, 142–148. [Google Scholar] [CrossRef] [PubMed]
- vanEngelsdorp, D.; Tarpy, D.R.; Lengerich, E.J.; Pettis, J.S. Idiopathic brood disease syndrome and queen events as precursors of colony mortality in migratory beekeeping operations in the eastern United States. Prev. Vet. Med. 2013, 108, 225–233. [Google Scholar] [CrossRef] [Green Version]
- Liu, Z.; Chen, C.; Niu, Q.; Qi, W.; Yuan, C.; Su, S.; Liu, S.; Zhang, Y.; Zhang, X.; Ji, T.; et al. Survey results of honey bee (Apis mellifera) colony losses in China (2010–2013). J. Apic. Res. 2016, 55, 29–37. [Google Scholar] [CrossRef]
- Rangel, J.; Keller, J.J.; Tarpy, D.R. The effects of honey bee (Apis mellifera L.) queen reproductive potential on colony growth. Insectes Soc. 2013, 60, 65–73. [Google Scholar] [CrossRef]
- Nelson, D.L.; Gary, N.E. Honey productivity of honeybee colonies in relation to body weight, attractiveness and fecundity of the queen. J. Apic. Res. 1983, 22, 209–213. [Google Scholar] [CrossRef]
- Oldroyd, B.P.; Goodman, R.D.; Allaway, M.A. On the relative importance of queens and workers to honey production. Apidologie 1990, 21, 153–159. [Google Scholar] [CrossRef] [Green Version]
- Tarpy, D.R. Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc. R. Soc. B 2003, 270, 99–103. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoopingarner, R.; Farrar, C. Genetic control of size in queen honey bees. J. Econ. Entomol. 1959, 52, 547–548. [Google Scholar] [CrossRef]
- Tarpy, D.R.; vanEngelsdorp, D.; Pettis, J.S. Genetic diversity affects colony survivorship in commercial honey bee colonies. Naturwissenschaften 2013, 100, 723–728. [Google Scholar] [CrossRef] [PubMed]
- De Souza, D.A.; Hartfelder, K.H.; Tarpy, D.R. Effects of larval age at grafting and juvenile hormone on morphometry and reproductive quality parameters of in vitro reared honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 2019, 112, 2030–2039. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.V.; Goblirsch, M.; McDermott, E.; Tarpy, D.R.; Spivak, M. Is the brood pattern within a honey bee colony a reliable indicator of queen quality? Insects 2019, 10, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sagili, R.R.; Metz, B.N.; Lucas, H.M.; Chakrabarti, P.; Breece, C.R. Honey bees consider larval nutritional status rather than genetic relatedness when selecting larvae for emergency queen rearing. Sci. Rep. 2018, 8, 7679. [Google Scholar] [CrossRef] [Green Version]
- Rangel, J.; Fisher, A. Factors affecting the reproductive health of honey bee (Apis mellifera) drones—A review. Apidologie 2019, 50, 759–778. [Google Scholar] [CrossRef] [Green Version]
- Fisher, A.; Rangel, J. Exposure to pesticides during development negatively affects honey bee (Apis mellifera) drone sperm viability. PLoS ONE 2018, 13, e0208630. [Google Scholar] [CrossRef]
- Kairo, G.; Provost, B.; Tchamitchian, S.; Ben Abdelkader, F.; Bonnet, M.; Cousin, M.; Sénéchal, J.; Benet, P.; Kretzschmar, A.; Belzunces, L.P.; et al. Drone exposure to the systemic insecticide Fipronil indirectly impairs queen reproductive potential. Sci. Rep. 2016, 6, 31904. [Google Scholar] [CrossRef] [Green Version]
- Payne, A.N.; Rangel, J. The effect of queen insemination volume on the growth of newly established honey bee (Apis mellifera) colonies. Apidologie 2018, 49, 594–605. [Google Scholar] [CrossRef] [Green Version]
- Mattila, H.R.; Seeley, T.D. Genetic diversity in honey bee colonies enhances productivity and fitness. Science 2007, 317, 362–364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zee, R.v.d.; Brodschneider, R.; Brusbardis, V.; Charrière, J.-D.; Chlebo, R.; Coffey, M.F.; Dahle, B.; Drazic, M.M.; Kauko, L.; Kretavicius, J.; et al. Results of international standardised beekeeper surveys of colony losses for winter 2012–2013: Analysis of winter loss rates and mixed effects modelling of risk factors for winter loss. J. Apic. Res. 2014, 53, 19–34. [Google Scholar] [CrossRef] [Green Version]
- Brodschneider, R.; Moosbeckhofer, R.; Crailsheim, K. Surveys as a tool to record winter losses of honey bee colonies: A two year case study in Austria and South Tyrol. J. Apic. Res. 2010, 49, 23–30. [Google Scholar] [CrossRef]
- Amiri, E.; Strand, M.K.; Rueppell, O.; Tarpy, D.R. Queen quality and the impact of honey bee diseases on queen health: Potential for interactions between two major threats to colony health. Insects 2017, 8, 48. [Google Scholar] [CrossRef]
- López, J.H.; Schuehly, W.; Crailsheim, K.; Riessberger-Gallé, U. Trans-generational immune priming in honeybees. Proc. R. Soc. B 2014, 281, 20140454. [Google Scholar] [CrossRef] [PubMed]
- Wei, H.; He, X.J.; Liao, C.H.; Wu, X.B.; Jiang, W.J.; Zhang, B.; Zhou, L.B.; Zhang, L.Z.; Barron, A.B.; Zeng, Z.J. A maternal effect on queen production in honeybees. Curr. Biol. 2019, 29, 2208–2213.e2203. [Google Scholar] [CrossRef]
- Preston, S.R.; Palmer, J.H.; Harrison, J.W.; Carr, H.M.; Rittschof, C.C. The impacts of maternal stress on worker phenotypes in the honey bee. Apidologie 2019, 50, 704–719. [Google Scholar] [CrossRef]
- Amiri, E.; Le, K.; Melendez, C.V.; Strand, M.K.; Tarpy, D.R.; Rueppell, O. Egg-size plasticity in Apis mellifera: Honey bee queens alter egg size in response to both genetic and environmental factors. J. Evol. Biol. 2020. [Google Scholar] [CrossRef]
- DeGrandi-Hoffman, G.; Chen, Y.; Simonds, R. The effects of pesticides on queen rearing and virus titers in honey bees (Apis mellifera L.). Insects 2013, 4, 71–89. [Google Scholar] [CrossRef] [Green Version]
- Rangel, J.; Tarpy, D.R. In-hive miticides and their effect on queen supersedure and colony growth in the honey bee (Apis mellifera). J. Environ. Anal. Toxicol. 2016, 6, 377. [Google Scholar] [CrossRef] [Green Version]
- Johnson, R.M.; Percel, E.G. Effect of a fungicide and spray adjuvant on queen-rearing success in honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 2013, 106, 1952–1957. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walsh, E.M.; Sweet, S.; Knap, A.; Ing, N.; Rangel, J. Queen honey bee (Apis mellifera) pheromone and reproductive behavior are affected by pesticide exposure during development. Behav. Ecol. Sociobiol. 2020, 74, 33. [Google Scholar] [CrossRef]
- Williams, G.R.; Troxler, A.; Retschnig, G.; Roth, K.; Yañez, O.; Shutler, D.; Neumann, P.; Gauthier, L. Neonicotinoid pesticides severely affect honey bee queens. Sci. Rep. 2015, 5, 14621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El-Niweiri, M.A.; Moritz, R.A. Mating in the rain? Climatic variance for polyandry in the honeybee (Apis mellifera jemenitica). Popul. Ecol. 2011, 53, 421–427. [Google Scholar] [CrossRef]
- Amiri, E.; Meixner, M.D.; Kryger, P. Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Sci. Rep. 2016, 6, 33065. [Google Scholar] [CrossRef] [PubMed]
- Pettis, J.S.; Rice, N.; Joselow, K.; vanEngelsdorp, D.; Chaimanee, V. Colony failure linked to low sperm viability in honey bee (Apis mellifera) queens and an exploration of potential causative factors. PLoS ONE 2016, 11, e0147220. [Google Scholar] [CrossRef]
- Withrow, J.M.; Pettis, J.S.; Tarpy, D.R. Effects of temperature during package transportation on queen establishment and survival in honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 2019, 112, 1043–1049. [Google Scholar] [CrossRef]
- Sandrock, C.; Tanadini, M.; Tanadini, L.G.; Fauser-Misslin, A.; Potts, S.G.; Neumann, P. Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure. PLoS ONE 2014, 9, e103592. [Google Scholar] [CrossRef] [Green Version]
- Chaimanee, V.; Pettis, J.S. Gene expression, sperm viability, and queen (Apis mellifera) loss following pesticide exposure under laboratory and field conditions. Apidologie 2019, 50, 304–316. [Google Scholar] [CrossRef]
- Wu-Smart, J.; Spivak, M. Sub-lethal effects of dietary neonicotinoid insecticide exposure on honey bee queen fecundity and colony development. Sci. Rep. 2016, 6, 32108. [Google Scholar] [CrossRef]
- Chaimanee, V.; Evans, J.D.; Chen, Y.; Jackson, C.; Pettis, J.S. Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. J. Insect Physiol. 2016, 89, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dussaubat, C.; Maisonnasse, A.; Crauser, D.; Tchamitchian, S.; Bonnet, M.; Cousin, M.; Kretzschmar, A.; Brunet, J.-L.; Le Conte, Y. Combined neonicotinoid pesticide and parasite stress alter honeybee queens’ physiology and survival. Sci. Rep. 2016, 6, 31430. [Google Scholar] [CrossRef] [PubMed]
- Brandt, A.; Grikscheit, K.; Siede, R.; Grosse, R.; Meixner, M.D.; Büchler, R. Immunosuppression in honeybee queens by the neonicotinoids Thiacloprid and Clothianidin. Sci. Rep. 2017, 7, 4673. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gauthier, L.; Ravallec, M.; Tournaire, M.; Cousserans, F.; Bergoin, M.; Dainat, B.; de Miranda, J.R. Viruses associated with ovarian degeneration in Apis mellifera L. queens. PLoS ONE 2011, 6, e16217. [Google Scholar] [CrossRef]
- Chen, Y.; Evans, J.; Feldlaufer, M. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J. Invertebr. Pathol. 2006, 92, 152–159. [Google Scholar] [CrossRef]
- Martin, S.J.; Highfield, A.C.; Brettell, L.; Villalobos, E.M.; Budge, G.E.; Powell, M.; Nikaido, S.; Schroeder, D.C. Global honey bee viral landscape altered by a parasitic mite. Science 2012, 336, 1304–1306. [Google Scholar] [CrossRef]
- Fries, I.; Camazine, S. Implications of horizontal and vertical pathogen transmission for honey bee epidemiology. Apidologie 2001, 32, 199–214. [Google Scholar] [CrossRef] [Green Version]
- Alizon, S.; Hurford, A.; Mideo, N.; Van Baalen, M. Virulence evolution and the trade-off hypothesis: History, current state of affairs and the future. J. Evol. Biol. 2009, 22, 245–259. [Google Scholar] [CrossRef]
- Shapiro-Ilan, D.I.; Fuxa, J.R.; Lacey, L.A.; Onstad, D.W.; Kaya, H.K. Definitions of pathogenicity and virulence in invertebrate pathology. J. Invertebr. Pathol. 2005, 88, 1–7. [Google Scholar] [CrossRef]
- Oldstone, M.B.A. Viral persistence: Parameters, mechanisms and future predictions. Virology 2006, 344, 111–118. [Google Scholar] [CrossRef]
- Lipsitch, M.; Siller, S.; Nowak, M.A. The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 1996, 50, 1729–1741. [Google Scholar] [CrossRef] [PubMed]
- de Miranda, J.R.; Fries, I. Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). J. Invertebr. Pathol. 2008, 98, 184–189. [Google Scholar] [CrossRef] [PubMed]
- Yue, C.; Schroder, M.; Gisder, S.; Genersch, E. Vertical-transmission routes for Deformed wing virus of honeybees (Apis mellifera). J. Gen. Virol. 2007, 88, 2329–2336. [Google Scholar] [CrossRef] [PubMed]
- Amiri, E.; Kryger, P.; Meixner, M.D.; Strand, M.K.; Tarpy, D.R.; Rueppell, O. Quantitative patterns of vertical transmission of deformed wing virus in honey bees. PLoS ONE 2018, 13, e0195283. [Google Scholar] [CrossRef]
- Ravoet, J.; De Smet, L.; Wenseleers, T.; de Graaf, D.C. Vertical transmission of honey bee viruses in a Belgian queen breeding program. BMC Vet. Res. 2015, 11, 1–6. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.; Pettis, J.S.; Collins, A.; Feldlaufer, M.F. Prevalence and transmission of honeybee viruses. Appl. Environ. Microbiol. 2006, 72, 606–611. [Google Scholar] [CrossRef] [Green Version]
- Shen, M.Q.; Cui, L.W.; Ostiguy, N.; Cox-Foster, D. Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and Sacbrood virus) with the honeybee host and the parasitic varroa mite. J. Gen. Virol. 2005, 86, 2281–2289. [Google Scholar] [CrossRef]
- Blanchard, P.; Ribiere, M.; Celle, O.; Lallemand, P.; Schurr, F.; Olivier, V.; Iscache, A.L.; Faucon, J.P. Evaluation of a real-time two-step RT-PCR assay for quantitation of Chronic bee paralysis virus (CBPV) genome in experimentally-infected bee tissues and in life stages of a symptomatic colony. J. Virol. Methods 2007, 141, 7–13. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.; Pettis, J.S.; Corona, M.; Chen, W.P.; Li, C.J.; Spivak, M.; Visscher, P.K.; DeGrandi-Hoffman, G.; Boncristiani, H.; Zhao, Y.; et al. Israeli acute paralysis virus: Epidemiology, pathogenesis and implications for honey bee health. PLoS Path. 2014, 10, e1004261. [Google Scholar] [CrossRef]
- Žvokelj, L.; Bakonyi, T.; Korošec, T.; Gregorc, A. Appearance of acute bee paralysis virus, black queen cell virus and deformed wing virus in Carnolian honey bee (Apis mellifera Carnica) queen rearing. J. Apic. Res. 2020, 59, 53–58. [Google Scholar] [CrossRef]
- Baily, L. The multiplication and spread of sacbrood virus of bees. Ann. Appl. Biol. 1969, 63, 483–491. [Google Scholar] [CrossRef] [PubMed]
- Maori, E.; Garbian, Y.; Kunik, V.; Mozes-Koch, R.; Malka, O.; Kalev, H.; Sabath, N.; Sela, I.; Shafir, S. A transmissible RNA pathway in honey bees. Cell Rep. 2019, 27, 1949–1959.E6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cox-Foster, D.L.; Conlan, S.; Holmes, E.C.; Palacios, G.; Evans, J.D.; Moran, N.A.; Quan, P.-L.; Briese, T.; Hornig, M.; Geiser, D.M.; et al. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 2007, 318, 283–287. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bailey, L.; Woods, R.D. Two more small RNA viruses from honey bees and further observations on Sacbrood and Acute bee-paralysis viruses. J. Gen. Virol. 1977, 37, 175–182. [Google Scholar] [CrossRef]
- Colwell, M.J.; Currie, R.W.; Pernal, S.F. Viruses in Unexpected Places: New Transmission Routes of European Honey Bee (Apis Mellifera) Viruses. In Proceedings of the 2017 American Bee Research Conference, Baton Rouge, LA, USA, 2 March 2017; p. 106. [Google Scholar]
- Di Prisco, G.; Pennacchio, F.; Caprio, E.; Boncristiani, H.F.; Evans, J.D.; Chen, Y. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J. Gen. Virol. 2011, 92, 151–155. [Google Scholar] [CrossRef]
- Shen, M.; Yang, X.; Cox-Foster, D.; Cui, L. The role of varroa mites in infections of Kashmir bee virus (KBV) and Deformed wing virus (DWV) in honey bees. Virology 2005, 342, 141–149. [Google Scholar] [CrossRef] [Green Version]
- 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 Oud. J. Invertebr. Pathol. 1999, 73, 101–106. [Google Scholar] [CrossRef] [Green Version]
- Harizanis, P.C. Infestation of queen cells by the mite Varroa jacobsoni. Apidologie 1991, 22, 533–538. [Google Scholar] [CrossRef]
- Williams, G.R.; Rogers, R.E.L.; Kalkstein, A.L.; Taylor, B.A.; Shutler, D.; Ostiguy, N. 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. 2009, 101, 77–79. [Google Scholar] [CrossRef]
- Prodělalová, J.; Moutelíková, R.; Titěra, D. Multiple virus infections in western honeybee (Apis mellifera L.) ejaculate used for instrumental insemination. Viruses 2019, 11, 306. [Google Scholar] [CrossRef] [Green Version]
- Yue, C.; Schroder, M.; Bienefeld, K.; Genersch, E. Detection of viral sequences in semen of honeybees (Apis mellifera): Evidence for vertical transmission of viruses through drones. J. Invertebr. Pathol. 2006, 92, 105–108. [Google Scholar] [CrossRef] [PubMed]
- Francis, R.M.; Nielsen, S.L.; Kryger, P. Varroa-virus interaction in collapsing honey bee colonies. PLoS ONE 2013, 8, e57540. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Miranda, J.R.; Genersch, E. Deformed wing virus. J. Invertebr. Pathol. 2010, 103, S48–S61. [Google Scholar] [CrossRef] [PubMed]
- Delaney, D.A.; Keller, J.J.; Caren, J.R.; Tarpy, D.R. The physical, insemination, and reproductive quality of honey bee queens (Apis mellifera L.). Apidologie 2011, 42, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Gregorc, A.; Bakonyi, T. Viral infections in queen bees (Apis mellifera carnica) from rearing apiaries. Acta Vet. Brno 2012, 81, 15–19. [Google Scholar] [CrossRef]
- Yañez, O.; Jaffé, R.; Jarosch, A.; Fries, I.; Moritz, R.F.A.; Paxton, R.J.; Miranda, J.R. Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): Implications for sexual transmission of a major honey bee virus. Apidologie 2012, 43, 17–30. [Google Scholar] [CrossRef] [Green Version]
- Gregorc, A.; Škerl, M.I.S. Characteristics of honey bee (Apis mellifera Carnica, Pollman 1879) queens reared in Slovenian commercial breeding stations. J. Apic. Sci. 2015, 59, 5–12. [Google Scholar] [CrossRef] [Green Version]
- Francis, R.M.; Nielsen, S.L.; Kryger, P. Patterns of viral infection in honey bee queens. J. Gen. Virol. 2013, 94, 668–676. [Google Scholar] [CrossRef]
- Amiri, E.; Seddon, G.; Zuluaga Smith, W.; Strand, M.K.; Tarpy, D.R.; Rueppell, O. Israeli acute paralysis virus: Honey bee queen–worker interaction and potential virus transmission pathways. Insects 2019, 10, 9. [Google Scholar] [CrossRef] [Green Version]
- Pankiw, T.; Winston, M.L.; Slessor, K.N. Queen attendance behavior of worker honey bees (Apis mellifera L.) that are high and low responding to queen mandibular pheromone. Insectes Soc. 1995, 42, 371–378. [Google Scholar] [CrossRef]
- Allen, M.D. Observations on honeybees attending their queen. Br. J. Anim. Behav. 1955, 3, 66–69. [Google Scholar] [CrossRef]
- Maori, E.; Navarro, I.C.; Boncristiani, H.; Seilly, D.J.; Rudolph, K.L.M.; Sapetschnig, A.; Lin, C.-C.; Ladbury, J.E.; Evans, J.D.; Heeney, J.L.; et al. A secreted RNA binding protein forms RNA-stabilizing granules in the honeybee royal jelly. Mol. Cell 2019, 74, 598–608.E6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Allen, M.D. The honeybee queen and her attendants. Anim. Behav. 1960, 8, 201–208. [Google Scholar] [CrossRef]
- Pham-Delegue, M.-H.; Trouiller, J.; Bakchine, E.; Roger, B.; Masson, C. Age dependency of worker bee response to queen pheromone in a four-armed olfactometer. Insectes Soc. 1991, 38, 283–292. [Google Scholar] [CrossRef]
- Chen, Y.; Siede, R. Honey bee viruses. In Advances in Virus Research; Maramorosch, K., Shabalina, S.A., Murphy, F.A., Eds.; Elsevier Academic Press Inc.: San Diego, CA, USA, 2007; Volume 70, pp. 33–80. [Google Scholar]
- McMenamin, A.J.; Flenniken, M.L. Recently identified bee viruses and their impact on bee pollinators. Curr. Opin. Insect Sci. 2018, 26, 120–129. [Google Scholar] [CrossRef]
- McMenamin, A.J.; Brutscher, L.M.; Glenny, W.; Flenniken, M.L. Abiotic and biotic factors affecting the replication and pathogenicity of bee viruses. Curr. Opin. Insect Sci. 2016, 16, 14–21. [Google Scholar] [CrossRef]
- de Miranda, J.R.; Cordoni, G.; Budge, G. The Acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J. Invertebr. Pathol. 2010, 103, S30–S47. [Google Scholar] [CrossRef]
- Ribiere, M.; Olivier, V.; Blanchard, P. Chronic bee paralysis: A disease and a virus like no other? J. Invertebr. Pathol. 2010, 103, 120–131. [Google Scholar] [CrossRef] [PubMed]
- Amiri, E.; Meixner, M.; Büchler, R.; Kryger, P. Chronic bee paralysis virus in honeybee queens: Evaluating susceptibility and infection routes. Viruses 2014, 6, 1188–1201. [Google Scholar] [CrossRef]
- Chen, Y.; Pettis, J.S.; Feldlaufer, M.F. Detection of multiple viruses in queens of the honey bee Apis mellifera L. J. Invertebr. Pathol. 2005, 90, 118–121. [Google Scholar] [CrossRef]
- Fievet, J.; Tentcheva, D.; Gauthier, L.; de Miranda, J.; 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. [Google Scholar] [CrossRef] [PubMed]
- Anderson, D.L.; Gibbs, A.J. Inapparent Virus infections and their interactions in pupae of the honey bee (Apis mellifera Linnaeus) in Australia. J. Gen. Virol. 1988, 69, 1617–1625. [Google Scholar] [CrossRef]
- Baracchi, D.; Fadda, A.; Turillazzi, S. Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J. Insect Physiol. 2012, 58, 1589–1596. [Google Scholar] [CrossRef] [Green Version]
- Natsopoulou, M.E.; McMahon, D.P.; Paxton, R. Parasites modulate within-colony activity and accelerate the temporal polyethism schedule of a social insect, the honey bee. Behav. Ecol. Sociobiol. 2016, 70, 1019–1031. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Galbraith, D.A.; Yang, X.; Niño, E.L.; Yi, S.; Grozinger, C. Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera). PLoS Path. 2015, 11, e1004713. [Google Scholar] [CrossRef] [Green Version]
- Tidbury, H.J.; Pedersen, A.B.; Boots, M. Within and transgenerational immune priming in an insect to a DNA virus. Proc. R. Soc. B 2011, 278, 871–876. [Google Scholar] [CrossRef] [Green Version]
- Büchler, R.; Andonov, S.; Bienefeld, K.; Costa, C.; Hatjina, F.; Kezic, N.; Kryger, P.; Spivak, M.; Uzunov, A.; Wilde, J. Standard methods for rearing and selection of Apis mellifera queens. J. Apic. Res. 2013, 52, 1–30. [Google Scholar] [CrossRef] [Green Version]
- Ståhlberg, A.; Bengtsson, M. Single-cell gene expression profiling using reverse transcription quantitative real-time PCR. Methods 2010, 50, 282–288. [Google Scholar] [CrossRef]
- Williams, G.R.; Alaux, C.; Costa, C.; Csáki, T.; Doublet, V.; Eisenhardt, D.; Fries, I.; Kuhn, R.; McMahon, D.P.; Medrzycki, P.; et al. Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. J. Apic. Res. 2013, 52. [Google Scholar] [CrossRef] [Green Version]
- Fine, J.D.; Shpigler, H.Y.; Ray, A.M.; Beach, N.J.; Sankey, A.L.; Cash-Ahmed, A.; Huang, Z.Y.; Astrauskaite, I.; Chao, R.; Zhao, H.; et al. Quantifying the effects of pollen nutrition on honey bee queen egg laying with a new laboratory system. PLoS ONE 2018, 13, e0203444. [Google Scholar] [CrossRef] [Green Version]
- Tetreau, G.; Dhinaut, J.; Gourbal, B.; Moret, Y. Trans-generational immune priming in invertebrates: Current knowledge and future prospects. Front. Immunol. 2019, 10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Amiri, E.; Strand, M.K.; Tarpy, D.R.; Rueppell, O. Honey Bee Queens and Virus Infections. Viruses 2020, 12, 322. https://doi.org/10.3390/v12030322
Amiri E, Strand MK, Tarpy DR, Rueppell O. Honey Bee Queens and Virus Infections. Viruses. 2020; 12(3):322. https://doi.org/10.3390/v12030322
Chicago/Turabian StyleAmiri, Esmaeil, Micheline K. Strand, David R. Tarpy, and Olav Rueppell. 2020. "Honey Bee Queens and Virus Infections" Viruses 12, no. 3: 322. https://doi.org/10.3390/v12030322