Traynor, K. S. et al. Varroa destructor: A complex parasite, crippling honey bees worldwide. Trends Parasitol. 36, 592–606. https://doi.org/10.1016/j.pt.2020.04.004 (2020).
Google Scholar
Rosenkranz, P., Aumeier, P. & Ziegelmann, B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, S96–S119. https://doi.org/10.1016/j.jip.2009.07.016 (2010).
Google Scholar
Noel, A., Le Conte, Y. & Mondet, F. Varroa destructor: how does it harm Apis mellifera honey bees and what can be done about it?. Emerg. Top. Life Sci. 4, 45–57. https://doi.org/10.1042/ETLS20190125 (2020).
Google Scholar
Boncristiani, H. et al. World honey bee health: the global distribution of western honey bee (Apis mellifera L.) pests and pathogens. Bee World 98, 2–6 (2020).
Google Scholar
Ramsey, S. D. et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc. Natl. Acad. Sci. U.S.A. 116, 1792–1801. https://doi.org/10.1073/pnas.1818371116 (2019).
Google Scholar
Di Prisco, G. et al. A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health. Proc. Natl. Acad. Sci. USA 113, 3203–3208. https://doi.org/10.1073/pnas.1523515113 (2016).
Google Scholar
Mondet, F. et al. Antennae hold a key to Varroa-sensitive hygiene behaviour in honey bees. Sci. Rep. 5, 10454. https://doi.org/10.1038/srep10454 (2015).
Google Scholar
McMenamin, A. J. & Genersch, E. Honey bee colony losses and associated viruses. Curr. Opin. Insect Sci. 8, 121–129. https://doi.org/10.1016/j.cois.2015.01.015 (2015).
Google Scholar
Beaurepaire, A. et al. Diversity and global distribution of viruses of the western honey bee Apis mellifera. Insects 11, 239. https://doi.org/10.3390/insects11040239 (2020).
Google Scholar
Levin, S. et al. New viruses from the ectoparasite mite Varroa destructor infesting Apis mellifera and Apis cerana. Viruses 11, 94. https://doi.org/10.3390/v11020094 (2019).
Google Scholar
Chen, G. et al. A new strain of virus discovered in China specific to the parasitic mite Varroa destructor poses a potential threat to honey bees. Viruses 13, 679. https://doi.org/10.3390/v13040679 (2021).
Google Scholar
Kraberger, S. et al. Genome sequences of two single-stranded DNA viruses identified in Varroa destructor. Genome Announc. 6, e00107-00118. https://doi.org/10.1128/genomeA.00107-18 (2018).
Google Scholar
Haddad, N., Horth, L., Al-Shagour, B., Adjlane, N. & Loucif-Ayad, W. Next-generation sequence data demonstrate several pathogenic bee viruses in Middle East and African honey bee subspecies (Apis mellifera syriaca, Apis mellifera intermissa) as well as their cohabiting pathogenic mites (Varroa destructor). Virus Genes 54, 694–705. https://doi.org/10.1007/s11262-018-1593-9 (2018).
Google Scholar
Wilfert, L. et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351, 594–597. https://doi.org/10.1126/science.aac9976 (2016).
Google Scholar
Remnant, E. J., Mather, N., Gillard, T. L., Yagound, B. & Beekman, M. Direct transmission by injection affects competition among RNA viruses in honeybees. Proc. Royal Soc. B 286, 20182452. https://doi.org/10.1098/rspb.2018.2452 (2019).
Google Scholar
Martin, S. J. & Brettell, L. E. Deformed wing virus in honeybees and other insects. Ann. Rev. Virol. 6, 49–69. https://doi.org/10.1146/annurev-virology-092818-015700 (2019).
Google Scholar
Martin, S. J. et al. Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–1306. https://doi.org/10.1126/science.1220941 (2012).
Google Scholar
Loope, K. J., Baty, J. W., Lester, P. J. & Wilson Rankin, E. E. Pathogen shifts in a honeybee predator following the arrival of the Varroa mite. Proc. Royal Soc. B 286, 20182499. https://doi.org/10.1098/rspb.2018.2499 (2019).
Google Scholar
McMahon, D. P. et al. Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. Royal Soc. B https://doi.org/10.1098/rspb.2016.0811 (2016).
Google Scholar
Grindrod, I., Kevill, J. L., Villalobos, E. M., Schroeder, D. C. & Ten Martin, S. J. years of Deformed wing virus (DWV) in Hawaiian honey bees (Apis mellifera), the dominant DWV-A variant is potentially being replaced by variants with a DWV-B coding sequence. Viruses 13, 969. https://doi.org/10.3390/v13060969 (2021).
Google Scholar
Kevill, J. L., Stainton, K. C., Schroeder, D. C. & Martin, S. J. Deformed wing virus variant shift from 2010 to 2016 in managed and feral UK honey bee colonies. Arch. Virol. 166, 2693–2702. https://doi.org/10.1007/s00705-021-05162-3 (2021).
Google Scholar
Grozinger, C. M. & Flenniken, M. L. Bee viruses: Ecology, pathogenicity, and impacts. Annu. Rev. Entomol. 64, 205–226. https://doi.org/10.1146/annurev-ento-011118-111942 (2019).
Google Scholar
Natsopoulou, M. E. et al. The virulent, emerging genotype B of Deformed wing virus is closely linked to overwinter honeybee worker loss. Sci. Rep. 7, 5242. https://doi.org/10.1038/s41598-017-05596-3 (2017).
Google Scholar
Iwasaki, J. M., Barratt, B. I., Lord, J. M., Mercer, A. R. & Dickinson, K. J. The New Zealand experience of varroa invasion highlights research opportunities for Australia. Ambio 44, 694–704. https://doi.org/10.1007/s13280-015-0679-z (2015).
Google Scholar
Solignac, M. et al. The invasive Korea and Japan types of Varroa destructor, ectoparasitic mites of the Western honeybee (Apis mellifera), are two partly isolated clones. Proc. Royal Soc. B 272, 411–419. https://doi.org/10.1098/rspb.2004.2853 (2005).
Google Scholar
Hall, R. J. et al. Apicultural practice and disease prevalence in Apis mellifera, New Zealand: A longitudinal study. J. Apic. Res. 60, 644–658. https://doi.org/10.1080/00218839.2021.1936422 (2021).
Google Scholar
Mondet, F., de Miranda, J. R., Kretzschmar, A., Le Conte, Y. & Mercer, A. R. On the front line: quantitative virus dynamics in honeybee (Apis mellifera L) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathog. 10, e1004323 (2014).
Google Scholar
McFadden, A. M. J. et al. Israeli acute paralysis virus not detected in Apis mellifera in New Zealand in a national survey. J. Apic. Res. 53, 520–527. https://doi.org/10.3896/ibra.1.53.5.03 (2015).
Google Scholar
Dobelmann, J., Felden, A. & Lester, P. J. Genetic strain diversity of multi-host RNA viruses that infect a wide range of pollinators and associates is shaped by geographic origins. Viruses 12, 358. https://doi.org/10.3390/v12030358 (2020).
Google Scholar
Gruber, M. A. M. et al. Single-stranded RNA viruses infecting the invasive argentine ant Linepithema humile. Sci. Rep. 7, 3304. https://doi.org/10.1038/s41598-017-03508-z (2017).
Google Scholar
Brenton-Rule, E. C. et al. The origins of global invasions of the German wasp (Vespula germanica) and its infection with four honey bee viruses. Biol. Invasions 20, 3445–3460. https://doi.org/10.1007/s10530-018-1786-0 (2018).
Google Scholar
Lester, P. J., Buick, K. H., Baty, J. W., Felden, A. & Haywood, J. Different bacterial and viral pathogens trigger distinct immune responses in a globally invasive ant. Sci. Rep. 9, 5780. https://doi.org/10.1038/s41598-019-41843-5 (2019).
Google Scholar
Lester, P. J. et al. No evidence of enemy release in pathogen and microbial communities of common wasps (Vespula vulgaris) in their native and introduced range. PLoS ONE 10, e0121358. https://doi.org/10.1371/journal.pone.0121358 (2015).
Google Scholar
Levin, S., Sela, N. & Chejanovsky, N. Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor. Sci. Rep. 6, 37710. https://doi.org/10.1038/srep37710 (2016).
Google Scholar
Cornman, S. R. et al. Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. BMC Genom. 11, 602. https://doi.org/10.1186/1471-2164-11-602 (2010).
Google Scholar
Gauthier, L. et al. The Apis mellifera filamentous virus genome. Viruses 7, 3798–3815. https://doi.org/10.3390/v7072798 (2015).
Google Scholar
Giuffre, C., Lubkin, S. R. & Tarpy, D. R. Does viral load alter behavior of the bee parasite Varroa destructor?. PLoS ONE 14, e0217975. https://doi.org/10.1371/journal.pone.0217975 (2019).
Google Scholar
De Smet, L. et al. BeeDoctor, a versatile MLPA-based diagnostic tool for screening bee viruses. PLoS ONE 7, e47953. https://doi.org/10.1371/journal.pone.0047953 (2012).
Google Scholar
Runckel, C. et al. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS ONE 6, e20656. https://doi.org/10.1371/journal.pone.0020656 (2011).
Google Scholar
Remnant, E. J. et al. A diverse range of novel RNA viruses in geographically distinct honey bee populations. J. Virol. 91, e00158. https://doi.org/10.1128/JVI.00158-17 (2017).
Google Scholar
Navajas, M. et al. New Asian types of Varroa destructor: a potential new threat for world apiculture. Apidologie 41, 181–193. https://doi.org/10.1051/apido/2009068 (2010).
Google Scholar
Kearse, M. et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199 (2012).
Google Scholar
Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755. https://doi.org/10.1093/bioinformatics/17.8.754 (2001).
Google Scholar
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. https://doi.org/10.1093/bioinformatics/btu170 (2014).
Google Scholar
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: A fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360. https://doi.org/10.1038/nmeth.3317 (2015).
Google Scholar
Wallberg, A. et al. A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosome-length scaffolds. BMC Genom. 20, 275. https://doi.org/10.1186/s12864-019-5642-0 (2019).
Google Scholar
Techer, M. A. et al. Divergent evolutionary trajectories following speciation in two ectoparasitic honey bee mites. Commun. Biol. 2, 357. https://doi.org/10.1038/s42003-019-0606-0 (2019).
Google Scholar
Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512. https://doi.org/10.1038/nprot.2013.084 (2013).
Google Scholar
Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using Diamond. Nat. Methods 12, 59–60. https://doi.org/10.1038/nmeth.3176 (2015).
Google Scholar
National Center for Biotechnology Information (NCBI). Bethesda (MD), National Library of Medicine (US), National Center for Biotechnology Information; [1988]–[cited 2017 Apr 06]. Available from: https://www.ncbi.nlm.nih.gov/.
Camacho, C. et al. BLAST+: Architecture and applications. BMC Bioinform. 10, 421. https://doi.org/10.1186/1471-2105-10-421 (2009).
Google Scholar
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419. https://doi.org/10.1038/nmeth.4197 (2017).
Google Scholar
R: A language and environment for statistical computing v. 4.0.2 (R Foundation for Statistical Computing, Vienna, Austria, 2020).
Oksanen, J. et al. vegan: community ecology package. (R package version 2.4–0. https://CRAN.R-project.org/package=vegan., 2016).
Li, D. et al. Molecular detection of small hive beetle Aethina tumida Murray (Coleoptera: Nitidulidae): DNA barcoding and development of a real-time PCR assay. Sci. Rep. 8, 9623. https://doi.org/10.1038/s41598-018-27603-x (2018).
Google Scholar
Anderson, D. L. & Trueman, J. W. H. Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp. Appl. Acarol. 24, 165–189. https://doi.org/10.1023/a:1006456720416 (2000).
Google Scholar
Bradford, E. L., Christie, C. R., Campbell, E. M. & Bowman, A. S. A real-time PCR method for quantification of the total and major variant strains of the Deformed wing virus. PLoS ONE 12, e0190017. https://doi.org/10.1371/journal.pone.0190017 (2017).
Google Scholar
Dynes, T. L. et al. Fine scale population genetic structure of Varroa destructor, an ectoparasitic mite of the honey bee (Apis mellifera). Apidologie 48, 93–101. https://doi.org/10.1007/s13592-016-0453-7 (2017).
Google Scholar
Maggi, M. et al. Genetic structure of Varroa destructor populations infesting Apis mellifera colonies in Argentina. Exp. Appl. Acarol. 56, 309–318. https://doi.org/10.1007/s10493-012-9526-0 (2012).
Google Scholar
Hasegawa, N., Techer, M. & Mikheyev, A. S. A toolkit for studying Varroa genomics and transcriptomics: preservation, extraction, and sequencing library preparation. BMC Genom. 22, 54. https://doi.org/10.1186/s12864-020-07363-7 (2021).
Google Scholar
Gisder, S. & Genersch, E. Direct evidence for infection of Varroa destructor mites with the bee-pathogenic Deformed wing virus variant B, but not variant A, via fluorescence in situ hybridization analysis. J. Virol. 95, e01786. https://doi.org/10.1128/JVI.01786-20 (2021).
Google Scholar
Gisder, S., Aumeier, P. & Genersch, E. Deformed wing virus: replication and viral load in mites (Varroa destructor). J. Gen. Virol. 90, 463–467. https://doi.org/10.1099/vir.0.005579-0 (2009).
Google Scholar
Yue, C. & Genersch, E. RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J. Gen. Virol. 86, 3419–3424. https://doi.org/10.1099/vir.0.81401-0 (2005).
Google Scholar
Posada-Florez, F. et al. Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner. Sci. Rep. 9, 12445. https://doi.org/10.1038/s41598-019-47447-3 (2019).
Google Scholar
Budge, G. E. et al. Chronic bee paralysis as a serious emerging threat to honey bees. Nat. Commun. 11, 2164. https://doi.org/10.1038/s41467-020-15919-0 (2020).
Google Scholar
Graystock, P. et al. The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. J. Appl. Ecol. 50, 1207–1215. https://doi.org/10.1111/1365-2664.12134 (2013).
Google Scholar
Roberts, J. M. K., Simbiken, N., Dale, C., Armstrong, J. & Anderson, D. L. Tolerance of honey bees to Varroa mite in the absence of deformed wing virus. Viruses https://doi.org/10.3390/v12050575 (2020).
Google Scholar
Brettell, L. E. & Martin, S. J. Oldest Varroa tolerant honey bee population provides insight into the origins of the global decline of honey bees. Sci. Rep. 7, 45953. https://doi.org/10.1038/srep45953 (2017).
Google Scholar
Herrero, S. et al. Identification of new viral variants specific to the honey bee mite Varroa destructor. Exp. Appl. Acarol. 79, 157–168. https://doi.org/10.1007/s10493-019-00425-w (2019).
Google Scholar
Dobelmann, J. et al. Fitness in invasive social wasps: the role of variation in viral load, immune response and paternity in predicting nest size and reproductive output. Oikos 126, 1208–1218. https://doi.org/10.1111/oik.04117 (2017).
Google Scholar
Shojaei, A., Nourian, A., Khanjani, M. & Mahmoodi, P. The first molecular characterization of Lake Sinai virus in honey bees (Apis mellifera) and Varroa destructor mites in Iran. J. Apic. Res. https://doi.org/10.1080/00218839.2021.1921467 (2021).
Google Scholar
Hartmann, U., Forsgren, E., Charriere, J. D., Neumann, P. & Gauthier, L. Dynamics of Apis mellifera filamentous Virus (AmFV) infections in honey bees and relationships with other parasites. Viruses 7, 2654–2667. https://doi.org/10.3390/v7052654 (2015).
Google Scholar
Nanetti, A., Bortolotti, L. & Cilia, G. Pathogens spillover from honey bees to other arthropods. Pathogens 10, 1044. https://doi.org/10.3390/pathogens10081044 (2021).
Google Scholar
Norton, A. M., Remnant, E. J., Buchmann, G. & Beekman, M. Accumulation and competition amongst Deformed wing virus genotypes in naive Australian honeybees provides insight into the increasing global prevalence of genotype B. Front. Microbiol. 11, 620. https://doi.org/10.3389/fmicb.2020.00620 (2020).
Google Scholar
Mordecai, G. J. et al. Superinfection exclusion and the long-term survival of honey bees in Varroa-infested colonies. ISME J. 10, 1182–1191. https://doi.org/10.1038/ismej.2015.186 (2016).
Google Scholar
Source: Ecology - nature.com