Effects of honey bee queen exposure to deformed wing virus-A on queen and juvenile infection and colony strength metrics

References

• Amiri, E., Kryger, P., Meixner, M. D., Strand, M. K., Tarpy, D. R., & Rueppell, O. (2018). Quantitative patterns of vertical transmission of deformed wing virus in honey bees. PLoS One, 13(3), e0195283. https://doi.org/10.1371/journal.pone.0195283
   PubMed Web of Science ®Google Scholar
• Amiri, E., Meixner, M., Büchler, R., & Kryger, P. (2014). Chronic bee paralysis virus in honeybee queens: Evaluating susceptibility and infection routes. Viruses, 6(3), 1188–1201. https://doi.org/10.3390/v6031188
   PubMed Web of Science ®Google Scholar
• Amiri, E., Meixner, M. D., & Kryger, P. (2016). Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Scientific Reports, 6(1), 33065. https://doi.org/10.1038/srep33065
   PubMedGoogle Scholar
• Amiri, E., Seddon, G., Zuluaga Smith, W., Strand, M. K., Tarpy, D. R., & Rueppell, O. (2019). Israeli acute paralysis virus: Honey bee queen–worker interaction and potential virus transmission pathways. Insects, 10(1), 9. https://doi.org/10.3390/insects10010009
   PubMed Web of Science ®Google Scholar
• Amiri, E., Strand, M. K., Rueppell, O., & Tarpy, D. R. (2017). Queen quality and the impact of honey bee diseases on queen health: Potential for interactions between two major threats to colony health. Insects, 8(2), 48. https://doi.org/10.3390/insects8020048
   PubMed Web of Science ®Google Scholar
• Amiri, E., Strand, M. K., Tarpy, D. R., & Rueppell, O. (2020). Honey bee queens and virus infections. Viruses, 12(3), 322. https://doi.org/10.3390/v12030322
   PubMed Web of Science ®Google Scholar
• Barribeau, S. M., & Schmid‐Hempel, P. (2017). Sexual healing: Mating induces a protective immune response in bumblebees. Journal of Evolutionary Biology, 30(1), 202–209. https://doi.org/10.1111/jeb.12964
   PubMed Web of Science ®Google Scholar
• Bhatia, S., Baral, S. S., Vega Melendez, C., Amiri, E., & Rueppell, O. (2021). Comparing survival of Israeli acute paralysis virus infection among stocks of US honey bees. Insects, 12(1), 60. https://doi.org/10.3390/insects12010060
   PubMed Web of Science ®Google Scholar
• Boncristiani, H. F., Evans, J. D., Chen, Y., Pettis, J., Murphy, C., Lopez, D. L., Simone-Finstrom, M., Strand, M., Tarpy, D. R., & Rueppell, O. (2013). In vitro infection of pupae with Israeli acute paralysis virus suggests disturbance of transcriptional homeostasis in honey bees (Apis mellifera). PloS One, 8(9), e73429. https://doi.org/10.1371/journal.pone.0073429
   PubMed Web of Science ®Google Scholar
• Bouuaert, D. C., De Smet, L., & de Graaf, D. C. (2021). Breeding for virus resistance and its effects on Deformed wing virus infection patterns in honey bee queens. Viruses, 13(6), 1074. https://doi.org/10.3390/v13061074
   PubMed Web of Science ®Google Scholar
• Büchler, R., Andonov, S., Bienefeld, K., Costa, C., Hatjina, F., Kezic, N., Kryger, P., Spivak, M., Uzunov, A., & Wilde, J. (2013). Standard methods for rearing and selection of Apis mellifera queens. Journal of Apicultural Research, 52(1), 1–30. https://doi.org/10.3896/IBRA.1.52.1.07
   Web of Science ®Google Scholar
• Calderone, N. W., Lin, S., & Kuenen, L. P. (2002). Differential infestation of honey bee, Apis mellifera, worker and queen brood by the parasitic mite Varroa destructor. Apidologie, 33(4), 389–398. https://doi.org/10.1051/apido:2002024
   Web of Science ®Google Scholar
• Chen, Y., Evans, J., & Feldlaufer, M. (2006). Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. Journal of Invertebrate Pathology, 92(3), 152–159. https://doi.org/10.1016/j.jip.2006.03.010
   PubMed Web of Science ®Google Scholar
• Chen, Y., Pettis, J. S., Collins, A., & Feldlaufer, M. F. (2006). Prevalence and transmission of honeybee viruses. Applied and Environmental Microbiology, 72(1), 606–611. https://doi.org/10.1128/AEM.72.1.606-611.2006
   PubMed Web of Science ®Google Scholar
• Chen, Y., Pettis, J. S., & Feldlaufer, M. F. (2005). Detection of multiple viruses in queens of the honey bee Apis mellifera L. Journal of Invertebrate Pathology, 90(2), 118–121. https://doi.org/10.1016/j.jip.2005.08.005
   PubMed Web of Science ®Google Scholar
• Cobey, S. W., Tarpy, D. R., & Woyke, J. (2013). Standard methods for instrumental insemination of Apis mellifera queens. Journal of Apicultural Research, 52(4), 1–18. https://doi.org/10.3896/IBRA.1.52.4.09
   Web of Science ®Google Scholar
• Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L., & Neumann, P. (2012). Dead or alive: Deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Applied and Environmental Microbiology, 78(4), 981–987. https://doi.org/10.1128/AEM.06537-11
   PubMed Web of Science ®Google Scholar
• de Miranda, J. R., Bailey, L., Ball, B. V., Blanchard, P., Budge, G. E., Chejanovsky, N., Chen, Y.-P., Gauthier, L., Genersch, E., de Graaf, D. C., Ribière, M., Ryabov, E., De Smet, L., & van der Steen, J. J. M. (2013). Standard methods for virus research in Apis mellifera. Journal of Apicultural Research, 52(4), 1–56. https://doi.org/10.3896/IBRA.1.52.4.22
   Web of Science ®Google Scholar
• de Miranda, J., & Fries, I. (2008). Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.). Journal of Invertebrate Pathology, 98(2), 184–189. https://doi.org/10.1016/j.jip.2008.02.004
   PubMed Web of Science ®Google Scholar
• Delaplane, K. S., Dag, A., Danka, R. G., Freitas, B. M., Garibaldi, L. A., Goodwin, R. M., & Hormaza, J. I. (2013). Standard methods for estimating strength parameters of Apis mellifera colonies. Journal of Apicultural Research, 52(4), 1–28. https://doi.org/10.3896/IBRA.1.52.4.12
   Web of Science ®Google Scholar
• Di Prisco, G., Zhang, X., Pennacchio, F., Caprio, E., Li, J., Evans, J. D., DeGrandi-Hoffman, G., Hamilton, M., & Chen, Y. P. (2011). Dynamics of persistent and acute deformed wing virus infections in honey bees, Apis mellifera. Viruses, 3(12), 2425–2441. https://doi.org/10.3390/v3122425
   PubMed Web of Science ®Google Scholar
• Ellis, J. D., Evans, J. D., & Pettis, J. (2010). Colony losses, managed colony population decline, and Colony Collapse Disorder in the United States. Journal of Apicultural Research, 49(1), 134–136. https://doi.org/10.3896/IBRA.1.49.1.30
   Web of Science ®Google Scholar
• Ferrandon, D., Jung, A., Criqui, M. C., Lemaitre, B., Uttenweiler‐Joseph, S., Michaut, L., Reichhart, J. M., & Hoffmann, J. (1998). A drosomycin–GFP reporter transgene reveals a local immune response in Drosophila that is not dependent on the toll pathway. The EMBO Journal, 17(5), 1217–1227. https://doi.org/10.1093/emboj/17.5.1217
   PubMed Web of Science ®Google Scholar
• Fievet, J., Tentcheva, D., Gauthier, L., De Miranda, J., Cousserans, F., Colin, M. E., & Bergoin, M. (2006). Localization of deformed wing virus infection in queen and drone Apis mellifera L. Virology Journal, 3(1), 16. https://doi.org/10.1186/1743-422X-3-16
   PubMedGoogle Scholar
• Francis, R. M., Nielsen, S. L., & Kryger, P. (2013). Patterns of viral infection in honey bee queens. The Journal of General Virology, 94(Pt 3), 668–676. https://doi.org/10.1099/vir.0.047019-0
   PubMedGoogle Scholar
• Gauthier, L., Ravallec, M., Tournaire, M., Cousserans, F., Bergoin, M., Dainat, B., & de Miranda, J. R. (2011). Viruses associated with ovarian degeneration in Apis mellifera L. queens. PLOS One, 6(1), e16217. https://doi.org/10.1371/journal.pone.0016217
   PubMed Web of Science ®Google Scholar
• Genersch, E., von der Ohe, W., Kaatz, H., Schroeder, A., Otten, C., Büchler, R., Berg, S., Ritter, W., Mühlen, W., Gisder, S., Meixner, M., Liebig, G., & Rosenkranz, P. (2010). The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies. Apidologie, 41(3), 332–352. https://doi.org/10.1051/apido/2010014
   Web of Science ®Google Scholar
• Hou, Y., Zhang, H., Miranda, L., & Lin, S. (2010). Serious overestimation in quantitative PCR by circular (supercoiled) plasmid standard: Microalgal pcna as the model gene. PLoS One, 5(3), e9545. https://doi.org/10.1371/journal.pone.0009545
   PubMed Web of Science ®Google Scholar
• Keehnen, N. L., Rolff, J., Theopold, U., & Wheat, C. W. (2017). Insect antimicrobial defences: A brief history, recent findings, biases, and a way forward in evolutionary studies. In Advances in insect physiology (vol. 52, pp. 1–33). Elsevier.
   Google Scholar
• Kevill, J. L., de Souza, F. S., Sharples, C., Oliver, R., Schroeder, D. C., & Martin, S. J. (2019). DWV-A lethal to honey bees (Apis mellifera): A colony level survey of DWV variants (A, B, and C) in England, Wales, and 32 states across the US. Viruses, 11(5), 426. https://doi.org/10.3390/v11050426
   PubMed Web of Science ®Google Scholar
• Kevill, J. L., Lee, K., Goblirsch, M., McDermott, E., Tarpy, D. R., Spivak, M., & Schroeder, D. C. (2020). The pathogen profile of a honey bee queen does not reflect that of her workers. Insects, 11(6), 382. https://doi.org/10.3390/insects11060382
   Google Scholar
• Khongphinitbunjong, K., de Guzman, L. I., Tarver, M. R., Rinderer, T. E., Chen, Y., & Chantawannakul, P. (2015). Differential viral levels and immune gene expression in three stocks of Apis mellifera induced by different numbers of Varroa destructor. Journal of Insect Physiology, 72, 28–34. https://doi.org/10.1016/j.jinsphys.2014.11.005
   PubMed Web of Science ®Google Scholar
• Kocher, S., Tarpy, D., & Grozinger, C. (2010). The effects of mating and instrumental insemination on queen honey bee flight behaviour and gene expression. Insect Molecular Biology, 19(2), 153–162. https://doi.org/10.1111/j.1365-2583.2009.00965.x
   PubMed Web of Science ®Google Scholar
• Kulinčević, J. M., & Rothenbuhler, W. C. (1975). Selection for resistance and susceptibility to hairless-black syndrome in the honeybee. Journal of Invertebrate Pathology, 25(3), 289–295. https://doi.org/10.1016/0022-2011(75)90084-1
   PubMed Web of Science ®Google Scholar
• Lang, S., Simone-Finstrom, M., & Healy, K. (2022). Context-dependent viral transgenerational immune priming in honey bees (Hymenoptera: Apidae). Journal of Insect Science (Online), 22(1), 19 (1–5). https://doi.org/10.1093/jisesa/ieac001
   Web of Science ®Google Scholar
• Leponiemi, M., Amdam, G. V., & Freitak, D. (2021). Exposure to inactivated deformed wing virus leads to transgenerational coasts but not immune priming in honeybees (Apis mellifera). Frontiers in Ecology and Evolution, 9. https://doi.org/10.3389/fevo.2021.626670
   Google Scholar
• Liu, F., Huang, W., Wu, K., Qiu, Z., Huang, Y., & Ling, E. (2017). Exploiting innate immunity for biological pest control. In Advances in insect physiology (vol. 52, pp. 199–230). Elsevier.
   Google Scholar
• Manfredini, F., Brown, M. J., Vergoz, V., & Oldroyd, B. P. (2015). RNA-sequencing elucidates the regulation of behavioural transitions associated with the mating process in honey bee queens. BMC Genomics, 16(1), 563. https://doi.org/10.1186/s12864-015-1750-7
   PubMedGoogle Scholar
• Martin, S. J., Highfield, A. C., Brettell, L., Villalobos, E. M., Budge, G. E., Powell, M., Nikaido, S., & Schroeder, D. C. (2012). Global honey bee viral landscape altered by a parasitic mite. Science (New York, N.Y.), 336(6086), 1304–1306. https://doi.org/10.1126/science.1220941
   PubMed Web of Science ®Google Scholar
• McMahon, D. P., Natsopoulou, M. E., Doublet, V., Fürst, M., Weging, S., Brown, M. J., Gogol-Döring, A., & Paxton, R. J. (2016). Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proceedings of the Royal Society B: Biological Sciences, 283(1833), 20160811. https://doi.org/10.1098/rspb.2016.0811
   PubMed Web of Science ®Google Scholar
• Möckel, N., Gisder, S., & Genersch, E. (2011). Horizontal transmission of deformed wing virus: Pathological consequences in adult bees (Apis mellifera) depend on the transmission route. The Journal of General Virology, 92(Pt 2), 370–377. https://doi.org/10.1099/vir.0.025940-0
   PubMedGoogle Scholar
• Norton, A. M., Remnant, E. J., Buchmann, G., & Beekman, M. (2020). Accumulation and competition amongst deformed wing virus genotypes in Naïve Australian Honeybees provides insight into the increasing global prevalence of genotype B. Frontiers in Microbiology, 11, 620. https://doi.org/10.3389/fmicb.2020.00620
   PubMed Web of Science ®Google Scholar
• Paxton, R. J., Schäfer, M. O., Nazzi, F., Zanni, V., Annoscia, D., Marroni, F., Bigot, D., Laws-Quinn, E. R., Panziera, D., Jenkins, C., & Shafiey, H. (2022). Epidemiology of a major honey bee pathogen, deformed wing virus: Potential worldwide replacement of genotype A by genotype B. International Journal for Parasitology. Parasites and Wildlife, 18, 157–171. https://doi.org/10.1016/j.ijppaw.2022.04.013
   PubMed Web of Science ®Google Scholar
• Peng, J., Zipperlen, P., & Kubli, E. (2005). Drosophila sex-peptide stimulates female innate immune system after mating via the Toll and Imd pathways. Current Biology: CB, 15(18), 1690–1694. https://doi.org/10.1016/j.cub.2005.08.048
   PubMed Web of Science ®Google Scholar
• Penn, H. J., Simone-Finstrom, M., Lang, S., Chen, J., & Healy, K. (2021). Host genotype and tissue type determine DWV infection intensity. Frontiers in Insect Science, 1, 756690. https://doi.org/10.3389/finsc.2021.756690
   Google Scholar
• Rinderer, T. E., Rothenbuhler, W. C., & Kulinčević, J. M. (1975). Responses of three genetically different stocks of the honeybee to a virus from bees with hairless-black syndrome. Journal of Invertebrate Pathology, 25(3), 297–300. https://doi.org/10.1016/0022-2011(75)90085-3
   Web of Science ®Google Scholar
• Ruttner, F. (1956). The mating of the honeybee. Bee World, 37(1), 3–15. https://doi.org/10.1080/0005772X.1956.11094913
   Google Scholar
• Ryabov, E. V., Childers, A. K., Chen, Y., Madella, S., Nessa, A., vanEngelsdorp, D., & Evans, J. D. (2017). Recent spread of Varroa destructor virus-1, a honey bee pathogen, in the United States. Scientific Reports, 7(1), 17447. https://doi.org/10.1038/s41598-017-17802-3
   PubMed Web of Science ®Google Scholar
• Schöning, C., Gisder, S., Geiselhardt, S., Kretschmann, I., Bienefeld, K., Hilker, M., & Genersch, E. (2012). Evidence for damage-dependent hygienic behaviour towards Varroa destructor-parasitised brood in the western honey bee, Apis mellifera. The Journal of Experimental Biology, 215(Pt 2), 264–271. https://doi.org/10.1242/jeb.062562
   PubMed Web of Science ®Google Scholar
• Seitz, N., Traynor, K. S., Steinhauer, N., Rennich, K., Wilson, M. E., Ellis, J. D., Rose, R., Tarpy, D. R., Sagili, R. R., Caron, D. M., Delaplane, K. S., Rangel, J., Lee, K., Baylis, K., Wilkes, J. T., Skinner, J. A., Pettis, J. S., & vanEngelsdorp, D. (2015). A national survey of managed honey bee 2014–2015 annual colony losses in the USA. Journal of Apicultural Research, 54(4), 292–304. https://doi.org/10.1080/00218839.2016.1153294
   Web of Science ®Google Scholar
• Simone-Finstrom, M., Aronstein, K., Goblirsch, M., Rinkevich, F., & de Guzman, L. (2018). Gamma irradiation inactivates honey bee fungal, microsporidian, and viral pathogens and parasites. Journal of Invertebrate Pathology, 153, 57–64. https://doi.org/10.1016/j.jip.2018.02.011
   PubMed Web of Science ®Google Scholar
• 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. Applied and Environmental Microbiology, 70(12), 7185–7191. https://doi.org/10.1128/AEM.70.12.7185-7191.2004
   PubMed Web of Science ®Google Scholar
• Traynor, K. S., Rennich, K., Forsgren, E., Rose, R., Pettis, J., Kunkel, G., Madella, S., Evans, J., Lopez, D., & vanEngelsdorp, D. (2016). Multiyear survey targeting disease incidence in US honey bees. Apidologie, 47(3), 325–347. https://doi.org/10.1007/s13592-016-0431-0
   Web of Science ®Google Scholar
• Tzou, P., Ohresser, S., Ferrandon, D., Capovilla, M., Reichhart, J.-M., Lemaitre, B., Hoffmann, J. A., & Imler, J.-L. (2000). Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity, 13(5), 737–748. https://doi.org/10.1016/s1074-7613(00)00072-8
   PubMed Web of Science ®Google Scholar
• Wagoner, K., Spivak, M., Hefetz, A., Reams, T., & Rueppell, O. (2019). Stock-specific chemical brood signals are induced by Varroa and Deformed Wing Virus, and elicit hygienic response in the honey bee. Scientific Reports, 9(1), 8753. https://doi.org/10.1038/s41598-019-45008-2
   PubMed Web of Science ®Google Scholar
• Weaver, D. B., Cantarel, B. L., Elsik, C. G., Boncristiani, D. L., & Evans, J. D. (2021). Multi-tiered analyses of honey bees that resist or succumb to parasitic mites and viruses. BMC Genomics, 22(1), 720. https://doi.org/10.1186/s12864-021-08032-z
   PubMed Web of Science ®Google Scholar
• Wilfert, L., Long, G., Leggett, H., Schmid-Hempel, P., Butlin, R., Martin, S., & Boots, M. (2016). Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science (New York, N.Y.), 351(6273), 594–597. https://doi.org/10.1126/science.aac9976
   PubMed Web of Science ®Google Scholar
• Winston, M. L. (1991). The biology of the honey bee. Harvard University Press.
   Google Scholar
• Yañez, O., Jaffé, R., Jarosch, A., Fries, I., Moritz, R. F., Paxton, R. J., & de Miranda, J. R. (2012). Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): implications for sexual transmission of a major honey bee virus. Apidologie, 43(1), 17–30. https://doi.org/10.1007/s13592-011-0088-7
   Web of Science ®Google Scholar
• Yañez, O., Piot, N., Dalmon, A., de Miranda, J. R., Chantawannakul, P., Panziera, D., Amiri, E., Smagghe, G., Schroeder, D., & Chejanovsky, N. (2020). Bee viruses: Routes of infection in hymenoptera. Frontiers in Microbiology, 11, 943. https://doi.org/10.3389/fmicb.2020.00943
   PubMed Web of Science ®Google Scholar
• Yue, C., & Genersch, E. (2005). RT-PCR analysis of deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). The Journal of General Virology, 86(Pt 12), 3419–3424. https://doi.org/10.1099/vir.0.81401-0
   PubMedGoogle Scholar
• Yue, C., Schröder, M., Gisder, S., & Genersch, E. (2007). Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). The Journal of General Virology, 88(Pt 8), 2329–2336. https://doi.org/10.1099/vir.0.83101-0
   PubMedGoogle Scholar