Abstract
Large-scale colony losses among managed Western honey bees have become a serious threat to the beekeeping industry in the last decade. Multiple factors contribute to these losses, but the impact of Varroa destructor parasitism is by far the most important, along with the contribution of some pathogenic viruses vectored by the mite. So far, more than 20 viruses have been identified infecting the honey bee, most of them RNA viruses. They may be maintained either as covert infections or causing severe symptomatic infections, compromising the viability of the colony. In silico analysis of available transcriptomic data obtained from mites collected in the USA and Europe, as well as additional investigation with new samples collected locally, allowed the description of three RNA viruses, two of them variants of the previously described VDV-2 and VDV-3 and the other a new species reported here for the first time. Our results showed that these viruses were widespread among samples and that they were present in the mites as well as in the bees but with differences in the relative abundance and prevalence. However, we have obtained strong evidence showing that these three viruses were able to replicate in the mite, but not in the bee, suggesting that they are selectively infecting the mite. This opens the door to future applications that may help controlling the mite through biological control approaches.
Similar content being viewed by others
References
Boecking O, Genersch E (2008) Varroosis—the ongoing crisis in bee keeping. J Consum Prot Food Saf 3:221–228
Brodschneider R, Gray A, Adjlane N, Ballis A, Brusbardis V, Charrière J-D, Chlebo R, Coffey MF, Dahle B, de Graaf DC, Maja Dražić M, Evans G, Fedoriak M, Forsythe I, Gregorc A, Grzęda U, Hetzroni A, Kauko L, Kristiansen P, Martikkala M, Martín-Hernández R, Aurelio Medina-Flores C, Mutinelli F, Raudmets A, Ryzhikov V, Simon-Delso N, Stevanovic J, Uzunov A, Vejsnæs F, Wöhl S, Zammit-Mangion M, Danihlík J (2018) Multi-country loss rates of honey bee colonies during winter 2016/2017 from the COLOSS survey. J Apicult Res 57:452–457
Campbell EM, McIntosh CH, Bowman AS (2016) A toolbox for quantitative gene expression in Varroa destructor: RNA degradation in field samples and systematic analysis of reference gene stability. PLoS ONE 11:e0155640
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics (Oxford, England) 25:1972–1973
De Jong D, De Jong PH, Gonçalves LS (1982) Weight loss and other damage to developing worker honeybees from infestation with Varroa jacobsoni. J Apicult Res 21:165–167
Di Prisco G, Pennacchio F, Caprio E, Boncristiani HF Jr, Evans JD, Chen Y (2011) Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J Gen Virol 92:151–155
Di Prisco G, Annoscia D, Margiotta M, Ferrara R, Varricchio P, Zanni V, Caprio E, Nazzi F, Pennacchio F (2016) 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
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Harvey E, Rose K, Eden J-S, Lo N, Abeyasuriya T, Shi M, Doggett SL, Holmes EC (2019) Extensive diversity of RNA viruses in australian ticks. J Virol 93:e01358-18
Jakubowska AK, Nalcacioglu R, Millan-Leiva A, Sanz-Carbonell A, Muratoglu H, Herrero S, Demirbag Z (2015) In search of pathogens: transcriptome-based identification of viral sequences from the pine processionary moth (Thaumetopoea pityocampa). Viruses 7:456–479
Levin S, Sela N, Chejanovsky N (2016) Two novel viruses associated with the Apis mellifera pathogenic mite Varroa destructor. Sci Rep 6:37710
Levin S, Sela N, Erez T, Nestel D, Pettis J, Neumann P, Chejanovsky N (2019) New viruses from the ectoparasite mite Varroa destructor Infesting Apis mellifera and Apis cerana. Viruses 11:94
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 − ΔΔCT method. Methods 25:402–408
Llopis-Giménez A, María González R, Millán-Leiva A, Catalá M, Llacer E, Urbaneja A, Herrero S (2017) Novel RNA viruses producing simultaneous covert infections in Ceratitis capitata. Correlations between viral titers and host fitness, and implications for SIT programs. J Invertebr Pathol 143:50–60
Longueville J-E, Lefort V, Gascuel O (2017) SMS: smart model selection in PhyML. Mol Biol Evol 34:2422–2424
McMenamin AJ, Genersch E (2015) Honey bee colony losses and associated viruses. Curr Opin Insect Sci 8:121–129
Nijveen H, Leunissen JAM, Geurts R, Bisseling T, Rao X, Untergasser A (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74
Ongus JR, Peters D, Bonmatin JM, Bengsch E, Vlak JM, van Oers MM (2004) Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J Gen Virol 85:3747–3755
Pettersson JHO, Shi M, Bohlin J, Eldholm V, Brynildsrud OB, Paulsen KM, Andreassen Å, Holmes EC (2017) Characterizing the virome of Ixodes ricinus ticks from northern Europe. Sci Rep 7:10870
Ramsey SD, Ochoa R, Bauchan G, Gulbronson C, Mowery JD, Cohen A, Lim D, Joklik J, Cicero JM, Ellis JD, Hawthorne D, vanEngelsdorp D (2019) Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc Natl Acad Sci USA 116:1792–1801
Roberts JMK, Anderson DL, Durr PA (2017) Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Sci Rep 7:6925
Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119
Sadeghi M, Altan E, Deng X, Barker CM, Fang Y, Coffey LL, Delwart E (2018) Virome of > 12 thousand Culex mosquitoes from throughout California. Virology 523:74–88
Santillán-Galicia MT, Ball BV, Clark SJ, Alderson PG (2014) Slow bee paralysis virus and its transmission in honey bee pupae by Varroa destructor. J Apicult Res 53:146–154
Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X, Li C-X, Qin X-C, Li J, Cao J-P, Eden J-S, Buchmann J, Wang W, Xu J, Holmes EC, Zhang Y-Z (2016) Redefining the invertebrate RNA virosphere. Nature 540:539
Standley DM, Katoh K (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Steinhauer N, Kulhanek K, Antunez K, Human H, Chantawannakul P, Chauzat MP, vanEngelsdorp D (2018) Drivers of colony losses. Curr Opin Insect Sci 26:142–148
Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform 11:7
Valles SM, Chen Y, Firth AE, Guérin DMA, Hashimoto Y, Herrero S, de Miranda JR, Ryabov E, Consortium IR (2017) ICTV virus taxonomy profile: Iflaviridae. J Gen Virol 98:527–528
VanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, Frazier M, Frazier J, Cox-Foster D, Chen Y, Underwood R, Tarpy DR, Pettis JS (2009) Colony collapse disorder: a descriptive study. PLoS ONE 4:e6481
Webster CL, Longdon B, Lewis SH, Obbard DJ (2016) Twenty-five new viruses associated with the Drosophilidae (Diptera). Evol Bioinform Online 12:13–25
Yang XL, Cox-Foster DL (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci USA 102:7470–7475
Yang X, Cox-Foster D (2007) Effects of parasitization by Varroa destructor on survivorship and physiological traits of Apis mellifera in correlation with viral incidence and microbial challenge. Parasitology 134:405–412
Acknowledgements
Joel González-Cabrera was supported by the Spanish Ministry of Economy and Competitiveness, Ramón y Cajal Program (RYC-2013-13834). The work at the Universitat de València was funded by a grant from the Spanish Ministry of Economy and Competitiveness (CGL2015‐65025‐R, MINECO/FEDER, UE). Research at the Universitat de València of Stefano Parenti was possible thanks to the Erasmus + program from the EU. Finally, we thank Fernando Calatayud and Enrique Simó, from the local beekeeper association ‘apiADS’, for providing bees and mites.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10493_2019_425_MOESM3_ESM.docx
Supplementary material 3 Table S2. Accession number of viral sequences used in this work for phylogenetic reconstruction (DOCX 29 kb)
10493_2019_425_MOESM4_ESM.tif
Supplementary material 4 Figure S1. Phylogenetic analysis of the VDV-2. Maximum-likelihood phylogenetic tree of the putative RdRp amino acid sequences of Varroa destructor virus 2 and closely related members of the Iflaviridae and Dicistroviridae families. Values on blanches indicates the aLRT support. Branches with aLRT values <0.6 have been collapsed. The grey scale bar represents 0.2 amino acid substitution per site. Sequence accession identifiers are provided in Table S2 (TIFF 1204 kb)
Rights and permissions
About this article
Cite this article
Herrero, S., Millán-Leiva, A., Coll, S. et al. Identification of new viral variants specific to the honey bee mite Varroa destructor. Exp Appl Acarol 79, 157–168 (2019). https://doi.org/10.1007/s10493-019-00425-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-019-00425-w