{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T09:17:11Z","timestamp":1790759831710,"version":"4.1.0"},"reference-count":102,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2020,10,27]],"date-time":"2020-10-27T00:00:00Z","timestamp":1603756800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ethiopian Agricultural Research Institute","award":["33-13-17"],"award-info":[{"award-number":["33-13-17"]}]},{"DOI":"10.13039\/100004413","name":"International Foundation for Science","doi-asserted-by":"publisher","award":["1_B_6119"],"award-info":[{"award-number":["1_B_6119"]}],"id":[{"id":"10.13039\/100004413","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002749","name":"Belgian Science policy office","doi-asserted-by":"publisher","award":["1-1-B-6119-1"],"award-info":[{"award-number":["1-1-B-6119-1"]}],"id":[{"id":"10.13039\/501100002749","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Ghent University Bijzonder Onderzoeksfonds","award":["001W14316"],"award-info":[{"award-number":["001W14316"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Metagenomics studies have accelerated the discovery of novel or divergent viruses of the honey bee. However, most of these studies predominantly focused on RNA viruses, and many suffer from the relatively low abundance of viral nucleic acids in the samples (i.e., compared to that of the host). Here, we explored the virome of the Ethiopian honey bee, Apis mellifera simensis, using an unbiased metagenomic approach in which the next-generation sequencing step was preceded by an enrichment protocol for viral particles. Our study revealed five well-known bee viruses and 25 atypical virus species, most of which have never been found in A. mellifera before. The viruses belong to Iflaviridae, Dicistroviridae, Secoviridae, Partitiviridae, Parvoviridae, Potyviridae, and taxonomically unclassified families. Fifteen of these atypical viruses were most likely plant-specific, and the remaining ten were presumed to be insect-specific. Apis mellifera filamentous virus (AmFV) was found in one sampling site out of 10. Two samples contained high read counts of a virus similar to Diatraea saccharales densovirus (DsDNV), which is a virus that causes high mortality in the sugarcane borer. AmFV and the DsDNV-like virus were the only DNA viruses found. Three viruses that primarily infect Drosophila spp. were also discovered: La Jolla virus (LJV), Kilifi virus (KiV), and Thika virus. Our study suggests that phoretic varroa mites are involved in the transmission of LJV and KiV and that both viruses replicate in mites and adult bees. We also found an overwhelming dominance of the deformed wing virus type B variant, which fits well with the apparently harmless infestation by Varroa destructor. It was suggested that Ethiopian bees have developed tolerance against virus infections as the result of natural selection.<\/jats:p>","DOI":"10.3390\/v12111218","type":"journal-article","created":{"date-parts":[[2020,10,28]],"date-time":"2020-10-28T11:43:06Z","timestamp":1603885386000},"page":"1218","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":32,"title":["Metagenomic Approach with the NetoVIR Enrichment Protocol Reveals Virus Diversity within Ethiopian Honey Bees (Apis mellifera simensis)"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8565-6065","authenticated-orcid":false,"given":"Haftom","family":"Gebremedhn","sequence":"first","affiliation":[{"name":"Laboratory of Molecular Entomology and Bee Pathology, Ghent University, B-9000 Ghent, Belgium"},{"name":"Tigray Agricultural Research Institute, P.O. Box 492 Mekelle, Ethiopia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3829-1056","authenticated-orcid":false,"given":"Ward","family":"Deboutte","sequence":"additional","affiliation":[{"name":"Laboratory of Viral Metagenomics, Laboratory for Clinical and Epidemiological Virology, Rega Institute, Department of Microbiology, Immunology and Transplantation, University of Leuven, B-3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7616-7630","authenticated-orcid":false,"given":"Karel","family":"Schoonvaere","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Entomology and Bee Pathology, Ghent University, B-9000 Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Demaeght","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Entomology and Bee Pathology, Ghent University, B-9000 Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lina","family":"De Smet","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Entomology and Bee Pathology, Ghent University, B-9000 Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bezabeh","family":"Amssalu","sequence":"additional","affiliation":[{"name":"Holeta Bee Research Center, P.O. Box 22 Holeta, Ethiopia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jelle","family":"Matthijnssens","sequence":"additional","affiliation":[{"name":"Laboratory of Viral Metagenomics, Laboratory for Clinical and Epidemiological Virology, Rega Institute, Department of Microbiology, Immunology and Transplantation, University of Leuven, B-3000 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8817-0781","authenticated-orcid":false,"given":"Dirk C.","family":"de Graaf","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Entomology and Bee Pathology, Ghent University, B-9000 Ghent, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,10,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"810","DOI":"10.1016\/j.ecolecon.2008.06.014","article-title":"Economic valuation of the vulnerability of world agriculture confronted with pollinator decline","volume":"68","author":"Gallai","year":"2009","journal-title":"Ecol. Econ."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Calderone, N.W. (2012). Insect Pollinated Crops, Insect Pollinators and US Agriculture: Trend Analysis of Aggregate Data for the Period 1992\u20132009. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0037235"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1098\/rspb.2006.3721","article-title":"Importance of pollinators in changing landscapes for world crops","volume":"274","author":"Klein","year":"2007","journal-title":"Proc. R. Soc. B Boil. Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1080\/00218839.2019.1615661","article-title":"Loss rates of honey bee colonies during winter 2017\/18 in 36 countries participating in the COLOSS survey, including effects of forage sources","volume":"58","author":"Gray","year":"2019","journal-title":"J. Apic. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"115","DOI":"10.3896\/IBRA.1.51.1.14","article-title":"A national survey of managed honey bee 2010\u201411 winter colony losses in the USA: Results from the Bee Informed Partnership","volume":"51","author":"VanEngelsdorp","year":"2012","journal-title":"J. Apic. Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1007\/s10393-013-0870-2","article-title":"Pathogens, Pests, and Economics: Drivers of Honey Bee Colony Declines and Losses","volume":"10","author":"Smith","year":"2013","journal-title":"Ecohealth"},{"key":"ref_7","first-page":"24","article-title":"The investigation of honey bee diseases after colony losses in Hatay and Adana provinces of Turkey","volume":"10","author":"Keskin","year":"2010","journal-title":"Mellifera"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1080\/0005772X.2005.11417323","article-title":"The worldwide health status of honey bees","volume":"86","author":"Ellis","year":"2005","journal-title":"Bee World"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"VanEngelsdorp, D., Hayes, J.H., Underwood, R.M., and Pettis, J. (2008). A survey of honey bee colony losses in the U.S. fall 2007 to spring 2008. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0004071"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Ravoet, J., Maharramov, J., Meeus, I., De Smet, L., Wenseleers, T., Smagghe, G., and de Graaf, D.C. (2013). Comprehensive Bee Pathogen Screening in Belgium Reveals Crithidia mellificae as a New Contributory Factor to Winter Mortality. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0072443"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1073\/pnas.1818371116","article-title":"Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph","volume":"116","author":"Ramsey","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3203","DOI":"10.1073\/pnas.1523515113","article-title":"A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health","volume":"113","author":"Annoscia","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1006\/jipa.1998.4807","article-title":"The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud","volume":"73","author":"Martin","year":"1999","journal-title":"J. Invertebr. Pathol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1099\/vir.0.025940-0","article-title":"Horizontal transmission of deformed wing virus: Pathological consequences in adult bees (Apis mellifera) depend on the transmission route","volume":"92","author":"Mockel","year":"2011","journal-title":"J. Gen. Virol."},{"key":"ref_15","first-page":"1","article-title":"Deformed wing virus type A, a major honey bee pathogen, is vectored by the mite Varroa destructor in a non-propagative manner","volume":"9","author":"Childers","year":"2019","journal-title":"Sci. Rep. UK"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.virol.2005.07.012","article-title":"The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees","volume":"342","author":"Shen","year":"2005","journal-title":"Virology"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1304","DOI":"10.1126\/science.1220941","article-title":"Global Honey Bee Viral Landscape Altered by a Parasitic Mite","volume":"336","author":"Martin","year":"2012","journal-title":"Science"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1099\/vir.0.005579-0","article-title":"Deformed wing virus: Replication and viral load in mites (Varroa destructor)","volume":"90","author":"Gisder","year":"2009","journal-title":"J. Gen. Virol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"S30","DOI":"10.1016\/j.jip.2009.06.014","article-title":"The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex","volume":"103","author":"Cordoni","year":"2010","journal-title":"J. Invertebr. Pathol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1051\/vetres\/2010027","article-title":"Emerging and re-emerging viruses of the honey bee (Apis mellifera L.)","volume":"41","author":"Genersch","year":"2010","journal-title":"Vet. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1146\/annurev-ento-011118-111942","article-title":"Bee Viruses: Ecology, Pathogenicity, and Impacts","volume":"64","author":"Grozinger","year":"2019","journal-title":"Annu. Rev. Entomol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.cois.2018.02.004","article-title":"Drivers of colony losses","volume":"26","author":"Steinhauer","year":"2018","journal-title":"Curr. Opin. Insect. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Francis, R.M., Nielsen, S.L., and Kryger, P. (2013). Varroa-Virus Interaction in Collapsing Honey Bee Colonies. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0057540"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/j.jip.2010.02.007","article-title":"First molecular detection of a viral pathogen in Ugandan honey bees","volume":"104","author":"Kajobe","year":"2010","journal-title":"J. Invertebr. Pathol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1007\/s13592-015-0372-z","article-title":"Discovery of Lake Sinai virus and an unusual strain of acute bee paralysis virus in West African apiaries","volume":"47","author":"Amakpe","year":"2016","journal-title":"Apidologie"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Muli, E., Patch, H., Frazier, M., Frazier, J., Torto, B., Baumgarten, T., Kilonzo, J., Kimani, J.N., Mumoki, F., and Masiga, D. (2014). Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in east Africa. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0094459"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1017\/S1742758417000212","article-title":"Prevalence of common honey bee pathogens at selected apiaries in Kenya, 2013\/2014","volume":"38","author":"Ongus","year":"2018","journal-title":"Int. J. Trop Insect. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"473","DOI":"10.4001\/003.022.0313","article-title":"An inventory of documented diseases of African honeybees","volume":"22","author":"Mumoki","year":"2014","journal-title":"Afr. Entomol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1007\/s13592-015-0406-6","article-title":"Honeybee health in Africa-a review","volume":"47","author":"Pirk","year":"2016","journal-title":"Apidologie"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1111\/1744-7917.12277","article-title":"Distribution and variability of deformed wing virus of honeybees (Apis mellifera) in the Middle East and North Africa","volume":"24","author":"Haddad","year":"2017","journal-title":"Insect Sci."},{"key":"ref_31","first-page":"1","article-title":"Investigating the viral ecology of global bee communities with high-throughput metagenomics","volume":"8","author":"Galbraith","year":"2018","journal-title":"Sci. Rep. UK"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e00158-17","DOI":"10.1128\/JVI.00158-17","article-title":"A Diverse Range of Novel RNA Viruses in Geographically Distinct Honey Bee Populations","volume":"91","author":"Remnant","year":"2017","journal-title":"J. Virol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"818","DOI":"10.1099\/jgv.0.001073","article-title":"Metagenomic analysis of Varroa-free Australian honey bees (Apis mellifera) shows a diverse Picornavirales virome","volume":"99","author":"Roberts","year":"2018","journal-title":"J. Gen. Virol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e0217822","DOI":"10.1371\/journal.pone.0217822","article-title":"RNA virus spillover from managed honeybees (Apis mellifera) to wild bumblebees (Bombus spp.)","volume":"14","author":"Alger","year":"2019","journal-title":"PLoS ONE"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.cois.2017.05.008","article-title":"The role of disease in bee foraging ecology","volume":"21","author":"Koch","year":"2017","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Aizenberg-Gershtein, Y., Izhaki, I., and Halpern, M. (2013). Do Honeybees Shape the Bacterial Community Composition in Floral Nectar?. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0067556"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"6827","DOI":"10.1002\/ece3.4197","article-title":"Impact of human disturbance on bee pollinator communities in savanna and agricultural sites in Burkina Faso, West Africa","volume":"8","author":"Stein","year":"2018","journal-title":"Ecol. Evol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Granberg, F., Vicente-Rubiano, M., Rubio-Guerri, C., Karlsson, O.E., Kukielka, D., Belak, S., and Sanchez-Vizcaino, J.M. (2013). Metagenomic Detection of Viral Pathogens in Spanish Honeybees: Co-Infection by Aphid Lethal Paralysis, Israel Acute Paralysis and Lake Sinai Viruses. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0057459"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.tim.2009.11.003","article-title":"New dimensions of the virus world discovered through metagenomics","volume":"18","author":"Kristensen","year":"2010","journal-title":"Trends Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"10511","DOI":"10.1073\/pnas.1921859117","article-title":"Honey-bee-associated prokaryotic viral communities reveal wide viral diversity and a profound metabolic coding potential","volume":"117","author":"Deboutte","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Schoonvaere, K., De Smet, L., Smagghe, G., Vierstraete, A., Braeckman, B.P., and de Graaf, D.C. (2016). Unbiased RNA Shotgun Metagenomics in Social and Solitary Wild Bees Detects Associations with Eukaryote Parasites and New Viruses. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0168456"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"177","DOI":"10.3389\/fmicb.2018.00177","article-title":"Study of the Metatranscriptome of Eight Social and Solitary Wild Bee Species Reveals Novel Viruses and Bee Parasites","volume":"9","author":"Schoonvaere","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1016\/j.jviromet.2013.08.035","article-title":"Evaluation of rapid and simple techniques for the enrichment of viruses prior to metagenomic virus discovery","volume":"195","author":"Hall","year":"2014","journal-title":"J. Virol. Methods"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"16532","DOI":"10.1038\/srep16532","article-title":"Modular approach to customise sample preparation procedures for viral metagenomics: A reproducible protocol for virome analysis","volume":"5","author":"Zeller","year":"2015","journal-title":"Sci. Rep. UK"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/978-1-4939-8682-8_7","article-title":"NetoVIR: Modular Approach to Customize Sample Preparation Procedures for Viral Metagenomics","volume":"1838","author":"Yinda","year":"2018","journal-title":"Methods Mol. Biol."},{"key":"ref_46","first-page":"1","article-title":"Standard methods for virus research in Apis mellifera","volume":"52","author":"Bailey","year":"2013","journal-title":"J. Apic. Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nmeth.3176","article-title":"Fast and sensitive protein alignment using DIAMOND","volume":"12","author":"Buchfink","year":"2015","journal-title":"Nat. Methods"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Ondov, B.D., Bergman, N.H., and Phillippy, A.M. (2011). Interactive metagenomic visualization in a Web browser. BMC Bioinform., 12.","DOI":"10.1186\/1471-2105-12-385"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","article-title":"Fast and accurate short read alignment with Burrows-Wheeler transform","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/s10493-008-9204-4","article-title":"Deformed wing virus associated with Tropilaelaps mercedesae infesting European honey bees (Apis mellifera)","volume":"47","author":"Forsgren","year":"2009","journal-title":"Exp. Appl. Acarol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2073","DOI":"10.1128\/AEM.00086-12","article-title":"Acaricide Treatment Affects Viral Dynamics in Varroa destructor-Infested Honey Bee Colonies via both Host Physiology and Mite Control (vol 78, pg 227, 2012)","volume":"78","author":"Locke","year":"2012","journal-title":"Appl. Environ. Microb."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.jviromet.2019.04.020","article-title":"Validation of quantitative real-time RT-PCR assays for the detection of six honeybee viruses","volume":"270","author":"Schurr","year":"2019","journal-title":"J. Virol. Methods"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability","volume":"30","author":"Katoh","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1972","DOI":"10.1093\/bioinformatics\/btp348","article-title":"trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses","volume":"25","author":"Gabaldon","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1093\/molbev\/msaa015","article-title":"IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era","volume":"37","author":"Minh","year":"2020","journal-title":"Mol. Biol. Evol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/nmeth.4285","article-title":"ModelFinder: Fast model selection for accurate phylogenetic estimates","volume":"14","author":"Kalyaanamoorthy","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1093\/molbev\/msx281","article-title":"UFBoot2: Improving the Ultrafast Bootstrap Approximation","volume":"35","author":"Hoang","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1093\/bioinformatics\/btq706","article-title":"phangorn: Phylogenetic analysis in R","volume":"27","author":"Schliep","year":"2011","journal-title":"Bioinformatics"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1111\/2041-210X.12628","article-title":"GGTREE: An R package for visualization and annotation of phylogenetic trees with their covariates and other associated data","volume":"8","author":"Yu","year":"2017","journal-title":"Methods Ecol. Evol."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"De Smet, L., Ravoet, J., de Miranda, J.R., Wenseleers, T., Mueller, M.Y., Moritz, R.F.A., and de Graaf, D.C. (2012). BeeDoctor, a Versatile MLPA-Based Diagnostic Tool for Screening Bee Viruses. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0047953"},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Webster, C.L., Waldron, F.M., Robertson, S., Crowson, D., Ferrari, G., Quintana, J.F., Brouqui, J.M., Bayne, E.H., Longdon, B., and Buck, A.H. (2015). The Discovery, Distribution, and Evolution of Viruses Associated with Drosophila melanogaster. PLoS Biol., 13.","DOI":"10.1101\/021154"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"D708","DOI":"10.1093\/nar\/gkx932","article-title":"Virus taxonomy: The database of the International Committee on Taxonomy of Viruses (ICTV)","volume":"46","author":"Lefkowitz","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1099\/vir.0.016667-0","article-title":"Self-priming of reverse transcriptase impairs strand-specific detection of dengue virus RNA","volume":"91","author":"Tuiskunen","year":"2010","journal-title":"J. Gen. Virol."},{"key":"ref_66","first-page":"3","article-title":"Occurrences and distributions of honeybee (Apis mellifera Jemenetica) varroa mite (Varroa destructor) in Tigray Region, Ethiopia","volume":"2","author":"Begna","year":"2014","journal-title":"J. Fish. Livest. Prod."},{"key":"ref_67","first-page":"4","article-title":"Identifying the species, effects and seasonal dynamics of honeybee varroa mites: A newly emerging parasite to Ethiopian honeybee","volume":"1","author":"Begna","year":"2016","journal-title":"Int. J. Sci. Res. Environ. Sci. Toxicol."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Gebremedhn, H., Amssalu, B., De Smet, L., and de Graaf, D.C. (2019). Factors restraining the population growth of Varroa destructor in Ethiopian honey bees (Apis mellifera simensis). PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0223236"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1101\/gr.226316.117","article-title":"Comprehensive viral enrichment enables sensitive respiratory virus genomic identification and analysis by next generation sequencing","volume":"28","author":"Li","year":"2018","journal-title":"Genome Res."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0042-6822(81)90247-6","article-title":"Properties of a Filamentous Virus of the Honey Bee (Apis-Mellifera)","volume":"114","author":"Bailey","year":"1981","journal-title":"Virology"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1080\/0005772X.1996.11099306","article-title":"The incidence and world distribution of honey bee viruses","volume":"77","author":"Allen","year":"1996","journal-title":"Bee World"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1007\/s11262-018-1593-9","article-title":"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)","volume":"54","author":"Haddad","year":"2018","journal-title":"Virus Genes"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Levin, S., Sela, N., Erez, T., Nestel, D., Pettis, J., Neumann, P., and Chejanovsky, N. (2019). New Viruses from the Ectoparasite Mite Varroa destructor Infesting Apis mellifera and Apis cerana. Viruses, 11.","DOI":"10.3390\/v11020094"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"3747","DOI":"10.1099\/vir.0.80470-0","article-title":"Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor","volume":"85","author":"Ongus","year":"2004","journal-title":"J. Gen. Virol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.virol.2011.05.009","article-title":"Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1-deformed wing virus recombinant (VDV-1-DWV) in the head of the honey bee","volume":"417","author":"Zioni","year":"2011","journal-title":"Virology"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1264","DOI":"10.1038\/ismej.2015.178","article-title":"Diversity in a honey bee pathogen: First report of a third master variant of the Deformed Wing Virus quasispecies","volume":"10","author":"Mordecai","year":"2016","journal-title":"ISME J."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Beaurepaire, A., Piot, N., Doublet, V., Antunez, K., Campbell, E., Chantawannakul, P., Chejanovsky, N., Gajda, A., Heerman, M., and Panziera, D. (2020). Diversity and Global Distribution of Viruses of the Western Honey Bee, Apis mellifera. Insects, 11.","DOI":"10.3390\/insects11040239"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"20160811","DOI":"10.1098\/rspb.2016.0811","article-title":"Elevated virulence of an emerging viral genotype as a driver of honeybee loss","volume":"283","author":"McMahon","year":"2016","journal-title":"Proc. R. Soc. B Boil. Sci."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Kevill, J.L., de Souza, F.S., Sharples, C., Oliver, R., Schroeder, D.C., and 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.","DOI":"10.3390\/v11050426"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1099\/vir.0.047019-0","article-title":"Patterns of viral infection in honey bee queens","volume":"94","author":"Francis","year":"2013","journal-title":"J. Gen. Virol."},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Amiri, E., Meixner, M., Nielsen, S.L., and Kryger, P. (2015). Four Categories of Viral Infection Describe the Health Status of Honey Bee Colonies. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0140272"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"6221","DOI":"10.1038\/s41598-019-42741-6","article-title":"Disentangling host-parasite-pathogen interactions in a varroa-resistant honeybee population reveals virus tolerance as an independent, naturally adapted survival mechanism","volume":"9","author":"Thaduri","year":"2019","journal-title":"Sci. Rep. UK"},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Locke, B., Forsgren, E., and de Miranda, J.R. (2014). Increased Tolerance and Resistance to Virus Infections: A Possible Factor in the Survival of Varroa destructor-Resistant Honey Bees (Apis mellifera). PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0099998"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1098\/rstb.2008.0184","article-title":"Decomposing health: Tolerance and resistance to parasites in animals","volume":"364","author":"Raberg","year":"2008","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.virusres.2014.04.007","article-title":"Taxonomic reorganization of family Partitiviridae and other recent progress in partitivirus research","volume":"188","author":"Nibert","year":"2014","journal-title":"Virus Res."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1099\/jgv.0.000985","article-title":"ICTV Virus Taxonomy Profile: Partitiviridae","volume":"99","author":"Vainio","year":"2018","journal-title":"J. Gen. Virol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"e00898-13","DOI":"10.1128\/mBio.00898-13","article-title":"Systemic Spread and Propagation of a Plant-Pathogenic Virus in European Honeybees, Apis mellifera","volume":"5","author":"Li","year":"2014","journal-title":"mBio"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1111\/aab.12461","article-title":"Honey bee-assisted surveillance for early plant virus detection","volume":"173","author":"Roberts","year":"2018","journal-title":"Ann. Appl. Biol."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1111\/ppa.12702","article-title":"The honeybee Apis mellifera contributes to Cucumber green mottle mosaic virus spread via pollination","volume":"67","author":"Darzi","year":"2018","journal-title":"Plant Pathol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/S0065-3527(08)60477-7","article-title":"Cryptic Plant-Viruses","volume":"32","author":"Boccardo","year":"1987","journal-title":"Adv. Virus Res."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1051\/agro:19870401","article-title":"Pea Seed-Borne Mosaic-Virus\u2014A Review","volume":"7","author":"Khetarpal","year":"1987","journal-title":"Agronomie"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.1007\/s00705-007-0966-5","article-title":"Molecular characterization and detection of Vicia cryptic virus in different Vicia faba cultivars","volume":"152","author":"Blawid","year":"2007","journal-title":"Arch. Virol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1071\/AP07050","article-title":"Plant pathogens transmitted by pollen","volume":"36","author":"Card","year":"2007","journal-title":"Australas. Plant Path."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1128\/JCM.01123-18","article-title":"Detection of Viruses in Clinical Samples by Use of Metagenomic Sequencing and Targeted Sequence Capture","volume":"56","author":"Wylie","year":"2018","journal-title":"J. Clin. Microbiol."},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Singh, R., Levitt, A.L., Rajotte, E.G., Holmes, E.C., Ostiguy, N., Vanengelsdorp, D., Lipkin, W.I., Depamphilis, C.W., Toth, A.L., and Cox-Foster, D.L. (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.","DOI":"10.1371\/journal.pone.0014357"},{"key":"ref_96","first-page":"13","article-title":"Twenty-Five New Viruses Associated with the Drosophilidae (Diptera)","volume":"12","author":"Webster","year":"2016","journal-title":"Evol. Bioinform."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.jip.2018.04.001","article-title":"Identification and characterization of natural viruses associated with the invasive insect pest Drosophila suzukii","volume":"154","author":"Carrau","year":"2018","journal-title":"J. Invertebr. Pathol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1159\/000149041","article-title":"Parvoviridae\u20142nd Report","volume":"11","author":"Bachmann","year":"1979","journal-title":"Intervirology"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.jip.2014.08.007","article-title":"Widespread occurrence of honey bee pathogens in solitary bees","volume":"122","author":"Ravoet","year":"2014","journal-title":"J. Invertebr. Pathol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1007\/s00248-015-0594-7","article-title":"Seasonal Variation of Honeybee Pathogens and its Association with Pollen Diversity in Uruguay","volume":"70","author":"Antunez","year":"2015","journal-title":"Microb. Ecol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1051\/apido\/2010014","article-title":"The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies","volume":"41","author":"Genersch","year":"2010","journal-title":"Apidologie"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1093\/nar\/gnf056","article-title":"Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification","volume":"30","author":"Schouten","year":"2002","journal-title":"Nucleic Acids Res."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/12\/11\/1218\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:29:22Z","timestamp":1760178562000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/12\/11\/1218"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,10,27]]},"references-count":102,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11]]}},"alternative-id":["v12111218"],"URL":"https:\/\/doi.org\/10.3390\/v12111218","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,10,27]]}}}