Abstract
Many viruses first isolated in honey bees can also infect and circulate in wild bee species. While most common bee viruses are generally less prevalent in wild bees than honey bees, they are occasionally locally common. However, most studies have not assessed prevalence of viruses in honey bees and wild bees at the same sites, making it difficult to determine how viruses may spread across species. We addressed this by surveying the prevalence of six viruses in honey bees and bumble bees at sites across the Pacific Northwest, USA. These data were used to assess covariance in virus prevalence between bee groups across multiple ecotypes and to assess how virus prevalence in bumble bees correlated with prevalence in honey bees. We show deformed wing virus (DWV) and black queen cell virus (BQCV) were more common in honey bees than bumble bees, while Israeli acute paralysis virus (IAPV) was found at similar levels. Prevalence of DWV and IAPV were correlated with landscape context, with both most common at urban sites. However, BQCV prevalence in bumble bees was best predicted by BQCV prevalence in honey bees and by apiary density. Our study provides evidence that several viruses are found in both honey bees and wild bumble bees at the same sites, although prevalence was not necessarily correlated among the two groups. Understanding the prevalence and impacts of bee viruses on both managed and wild bees is key for disease mitigation and pollinator conservation.
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Data and code are available at GitHub, https://github.com/verawp.
References
Alger SA, Burnham PA, Boncristiani HF, Brody AK (2019a) RNA virus spillover from managed honey bees (Apis mellifera) to wild bumble bees (Bombus spp.). PLoS ONE 14:e0217822
Alger SA, Burnham PA, Brody AK (2019b) Flowers as viral hot spots: honey bees (Apis mellifera) unevenly deposit viruses across plant species. PLoS ONE 14:e0221800
Bruckner S, Wilson M, Aurell D, Rennich K, vanEngelsdorp D, Steinhauer N, Williams GR (2023) A national survey of managed honey bee colony losses in the USA: results from the Bee Informed Partnership for 2017–18, 2018–19, and 2019–20. J Apic Res 1–15. https://doi.org/10.1080/00218839.2022.2158586
Berényi O, Bakonyi T, Derakhshifar I, Köglberger H, Nowotny N (2006) Occurrence of six honey bee viruses in diseased Austrian apiaries. Appl Environ Microbiol 72:2414–2420
Boncristiani H, Li J, Evans JD, Pettis J, Chen Y (2011) Scientific note on PCR inhibitors in the compound eyes of honey bees, Apis mellifera. Apidologie 42:457–460
Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D, Pettis JS, vanEngelsdorp D, Evans JD (2012) Pathogen webs in collapsing honey bee colonies. PLoS ONE 7:e43562
Dalmon A, Diévart V, Thomasson M, Fouque R, Vaissière BE, Guilbaud L, Le Conte Y, Henry M (2021) Possible spillover of pathogens between bee communities foraging on the same floral resource. InSects 12:122
Dolezal AG, Hendrix SD, Scavo NA, Carrillo-Tripp J, Harris MA, Wheelock MJ, O’Neal ME, Toth AL (2016) Honey bee viruses in wild bees: viral prevalence, loads, and experimental inoculation. PLoS ONE 11:e0166190
Fürst MA, McMahon DP, Osborne JL, Paxton RJ, Brown MJF (2014) Disease associations between honey bees and bumble bees as a threat to wild pollinators. Nature 506:364–366
Genersch E, Yue C, Fries I, de Miranda JR (2006) Detection of deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J Invert Pathol 91:61–63
Goulson D, Hughes WOH (2015) Mitigating the anthropogenic spread of bee parasites to protect wild pollinators. Biol Conserv 191:10–19
Grozinger CM, Flenniken ML (2019) Bee viruses: ecology, pathogenicity, and impacts. Annu Rev Entomol 64:205–226
Gusachenko ON, Woodford L, Balbirnie-Cumming K, Ryabov EV, Evans DJ (2020) Evidence for and against deformed wing virus spillover from honey bees to bumble bees: a reverse genetic analysis. Sci Reports 10:16847
Johnson PTJ, de Roode JC, Fenton A (2015) Why infectious disease research needs community ecology. Science 349:1259504–1259504
Levitt AL, Singh R, Cox-Foster DL, Rajotte E, Hoover K, Ostiguy N, Holmes EC (2013) Cross-species transmission of honey bee viruses in associated arthropods. Virus Res 176:232–240
Li J, Peng W, Wu J, Strange JP, Boncristiani H, Chen Y (2011) Cross-species infection of deformed wing virus poses a new threat to pollinator conservation. J Econ Entomol 104:732–739
Manley R, Temperton B, Doyle T, Gates D, Hedges S, Boots M, Wilfert L (2019) Knock-on community impacts of a novel vector: spillover of emerging DWV-B from Varroa-infested honey bees to wild bumble bees. Ecol Lett 22:1306–1315
McMahon DP, Fürst MA, Caspar J, Theodorou P, Brown MJF, Paxton RJ (2015) A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J Anim Ecol 84:615–624
Nanetti A, Bortolotti L, Cilia G (2021) Pathogens spillover from honey bees to other arthropods. Pathogens 1:1044
Otterstatter MC, Thomson JD (2008) Does pathogen spillover from commercially reared bumble bees threaten wild pollinators? PLoS ONE 3:e2771
Peng W, Li J, Boncristiani H, Strange JP, Hamilton M, Chen Y (2011) Host range expansion of honey bee black queen cell virus in the bumble bee, Bombus huntii. Apidologie 42:650–658
Pfeiffer VW, Crowder DW (2022) Factors affecting virus prevalence in honey bees in the Pacific-Northwest, USA. J Invertebr Pathol 187:107703
Purkiss T, Lach L (2019) Pathogen spillover from Apis mellifera to a stingless bee. Proc Roy Soc London Series B 286:20191071
Ravoet J, De Smet L, Meeus I, Smagghe G, Wenseleers T, de Graaf DC (2014) Widespread occurrence of honey bee pathogens in solitary bees. J Invertebr Pathol 122:55–58
Schläppi D, Lattrell P, Yañez O, Chejanovsky N, Neumann P (2019) Foodborne transmission of deformed wing virus to ants (Myrmica rubra). InSects 10:394
Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N, van Engelsdorp D, Lipkin WI, dePamphilis CW, Toth AL, Cox-Foster DL (2010) RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE 5:e14357
Tehel A, Brown MJ, Paxton RJ (2016) Impact of managed honey bee viruses on wild bees. Curr Opin Virol 19:16–22
Tehel A, Streicher T, Tragust S, Paxton RJ (2020) Experimental infection of bumble bees with honey bee-associated viruses: no direct fitness costs but potential future threats to novel wild bee hosts. Roy Soc Open Sci 7:200480
Woolhouse MEJ (2001) Population biology of multihost pathogens. Science 292:1109–1112
Acknowledgements
We thank O. Forrester for helping with the data analysis and Western SARE (grant SW18-031) for the funding.
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The research was funded by Western SARE (grant SW18-031).
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VP and DC contributed to the study conception and design. Lab analysis of samples was carried out by VP and SB. VP analyzed the data and drafted the manuscript. All authors read and approved the final manuscript.
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Pfeiffer, V.W., Basu, S. & Crowder, D.W. Patterns of virus coincidence between honey bees and bumble bees in the Pacific Northwest, USA. Apidologie 55, 30 (2024). https://doi.org/10.1007/s13592-024-01072-w
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DOI: https://doi.org/10.1007/s13592-024-01072-w