{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T20:00:00Z","timestamp":1790798400160,"version":"4.1.0"},"reference-count":56,"publisher":"National Academy of Sciences","issue":"26","license":[{"start":{"date-parts":[[2023,6,20]],"date-time":"2023-06-20T00:00:00Z","timestamp":1687219200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000923","name":"Australian Research Council","doi-asserted-by":"crossref","award":["FT160100178"],"award-info":[{"award-number":["FT160100178"]}],"id":[{"id":"10.13039\/501100000923","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2023,6,27]]},"abstract":"<jats:p>\n                    Novel transmission routes can allow infectious diseases to spread, often with devastating consequences. Ectoparasitic varroa mites vector a diversity of RNA viruses, having switched hosts from the eastern to western honey bees (\n                    <jats:italic>Apis cerana<\/jats:italic>\n                    to\n                    <jats:italic>Apis mellifera<\/jats:italic>\n                    ). They provide an opportunity to explore how novel transmission routes shape disease epidemiology. As the principal driver of the spread of deformed wing viruses (mainly DWV-A and DWV-B), varroa infestation has also driven global honey bee health declines. The more virulent DWV-B strain has been replacing the original DWV-A strain in many regions over the past two decades. Yet, how these viruses originated and spread remains poorly understood. Here, we use a phylogeographic analysis based on whole-genome data to reconstruct the origins and demography of DWV spread. We found that, rather than reemerging in western honey bees after varroa switched hosts, as suggested by previous work, DWV-A most likely originated in East Asia and spread in the mid-20th century. It also showed a massive population size expansion following the varroa host switch. By contrast, DWV-B was most likely acquired more recently from a source outside East Asia and appears absent from the original varroa host. These results highlight the dynamic nature of viral adaptation, whereby a vector\u2019s host switch can give rise to competing and increasingly virulent disease pandemics. The evolutionary novelty and rapid global spread of these host\u2013virus interactions, together with observed spillover into other species, illustrate how increasing globalization poses urgent threats to biodiversity and food security.\n                  <\/jats:p>","DOI":"10.1073\/pnas.2301258120","type":"journal-article","created":{"date-parts":[[2023,6,20]],"date-time":"2023-06-20T13:54:41Z","timestamp":1687269281000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":30,"title":["Evolutionarily diverse origins of deformed wing viruses in western honey bees"],"prefix":"10.1073","volume":"120","author":[{"given":"Nonno","family":"Hasegawa","sequence":"first","affiliation":[{"name":"Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5417-5103","authenticated-orcid":false,"given":"Maeva A.","family":"Techer","sequence":"additional","affiliation":[{"name":"Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan"},{"name":"Department of Entomology, Texas A&amp;M University, College Station, TX 77483"},{"name":"Behavioral Plasticity Research Institute, NSF-BII, College Station, TX 77483"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0369-2968","authenticated-orcid":false,"given":"Noureddine","family":"Adjlane","sequence":"additional","affiliation":[{"name":"Department of Agronomy, Faculty of Science, University M\u2019hamed Bougara, Boumerdes 35000, Algeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muntasser Sabah","family":"al-Hissnawi","sequence":"additional","affiliation":[{"name":"Ministry of Education, General Directorate of Education in Najaf Governorat, Najaf-Kufa 54003, Iraq"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karina","family":"Ant\u00fanez","sequence":"additional","affiliation":[{"name":"Departamento de Microbiolog\u00eda, Instituto de Investigaciones Biol\u00f3gicas Clemente Estable, 11600 Montevideo, Uruguay"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9832-5609","authenticated-orcid":false,"given":"Alexis","family":"Beaurepaire","sequence":"additional","affiliation":[{"name":"Swiss Bee Research Center, Agroscope, 3003 Bern, Switzerland"},{"name":"Institute of Bee Health, University of Bern, 3003 Bern, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Krisztina","family":"Christmon","sequence":"additional","affiliation":[{"name":"United States Department of Agriculture, Agricultural Research Service, Bee Research Lab, Beltsville, MD 20705"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helene","family":"Delatte","sequence":"additional","affiliation":[{"name":"Centre de coop\u00e9ration internationale en recherche agronomique pour le d\u00e9veloppement, UMR Unit\u00e9 Mixte de Recherche Peuplements V\u00e9g\u00e9taux et Bioagresseurs en Milieu Tropical, F-97410 Saint-Pierre, La R\u00e9union, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5578-7950","authenticated-orcid":false,"given":"Usman H.","family":"Dukku","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Abubakar Tafawa Balewa University, Bauchi 740211, Nigeria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nurit","family":"Eliash","sequence":"additional","affiliation":[{"name":"Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan"},{"name":"Shamir Research Institute, Haifa University, Haifa 3498838, Israel"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4021-9117","authenticated-orcid":false,"given":"Mogbel A. A.","family":"El-Niweiri","sequence":"additional","affiliation":[{"name":"Department of Bee Research, Environment, Natural Resources and Desertification Research Institute, National Centre for Research, Khartoum, Sudan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivier","family":"Esnault","sequence":"additional","affiliation":[{"name":"Groupement de D\u00e9fense Sanitaire, R\u00e9union, La plaine des Cafres 97418, La R\u00e9union, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0036-4651","authenticated-orcid":false,"given":"Jay D.","family":"Evans","sequence":"additional","affiliation":[{"name":"United States Department of Agriculture, Agricultural Research Service, Bee Research Lab, Beltsville, MD 20705"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nizar J.","family":"Haddad","sequence":"additional","affiliation":[{"name":"Bee Research Department, National Agricultural Research Center, 19381 Baqa\u2019, Jordan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6083-9981","authenticated-orcid":false,"given":"Barbara","family":"Locke","sequence":"additional","affiliation":[{"name":"Department of Ecology, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9234-3267","authenticated-orcid":false,"given":"Irene","family":"Mu\u00f1oz","sequence":"additional","affiliation":[{"name":"Department of Zoology and Physical Anthropology, Faculty of Veterinary, University of Murcia, 30100 Murcia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5994-1022","authenticated-orcid":false,"given":"Gr\u00e9goire","family":"No\u00ebl","sequence":"additional","affiliation":[{"name":"Functional and Evolutionary Entomology, TERRA, Gembloux Agro-Bio Tech, University of Li\u00e8ge, 5030 Gembloux, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Delphine","family":"Panziera","sequence":"additional","affiliation":[{"name":"Wageningen University &amp; Research, 6708 PB Wageningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9739-5595","authenticated-orcid":false,"given":"John M. K.","family":"Roberts","sequence":"additional","affiliation":[{"name":"Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT 2601, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0058-1402","authenticated-orcid":false,"given":"Pilar","family":"De la R\u00faa","sequence":"additional","affiliation":[{"name":"Department of Zoology and Physical Anthropology, Faculty of Veterinary, University of Murcia, 30100 Murcia, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4099-9846","authenticated-orcid":false,"given":"Mohamed A.","family":"Shebl","sequence":"additional","affiliation":[{"name":"Department of Plant Protection, Faculty of Agriculture, Suez Canal University, 41522 Ismailia, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2657-8591","authenticated-orcid":false,"given":"Zoran","family":"Stanimirovic","sequence":"additional","affiliation":[{"name":"Department of Biology, Faculty of Veterinary Medicine, University of Belgrade, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9457-7561","authenticated-orcid":false,"given":"David A.","family":"Rasmussen","sequence":"additional","affiliation":[{"name":"Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695"},{"name":"Bioinformatics Research Center, North Carolina State University, Raleigh, NC 27695"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4369-1019","authenticated-orcid":false,"given":"Alexander S.","family":"Mikheyev","sequence":"additional","affiliation":[{"name":"Research School of Biology, Australian National University, Canberra, ACT 2601, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2023,6,20]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature02759"},{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tim.2012.11.003"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.284.5418.1311"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.3201\/eid1112.050997"},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","DOI":"10.1093\/oso\/9780199211128.001.0001","volume-title":"The Evolution and Emergence of RNA Viruses","author":"Holmes E. 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Gisder E. Genersch Direct evidence for infection of Varroa destructor Mites with the bee-pathogenic deformed wing virus variant B\u2013but not variant A\u2013via fluorescence-in situ-hybridization analysis. J. Virol. 95 e01786-20 (2021). e01786-20","DOI":"10.1128\/JVI.01786-20"},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-47447-3"},{"key":"e_1_3_4_24_2","first-page":"20160811","article-title":"Elevated virulence of an emerging viral genotype as a driver of honeybee loss","volume":"283","author":"McMahon D. P.","year":"2016","unstructured":"D. P. McMahon , Elevated virulence of an emerging viral genotype as a driver of honeybee loss. Proc. R. Soc. 283, 20160811 (2016).","journal-title":"Proc. R. 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Aitchison, The statistical analysis of compositional data. J. R. Stat. Soc. 44, 139\u2013160 (1982).","journal-title":"J. R. Stat. Soc."},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","unstructured":"B. H. McArdle M. J. Anderson Fitting multivariate models to community data: A comment on distance\u2013based redundancy analysis. 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Deng An investigation of honey bee virus prevalence in managed honey bees (Apis mellifera and Apis cerana) undergone colony losses: A case study in China. Res. 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Manley , Knock-on community impacts of a novel vector: Spillover of emerging DWV-B from Varroa-infested honeybees to wild bumblebees. Ecol. Lett. 22, 1306\u20131315 (2019).","journal-title":"Ecol. Lett."},{"key":"e_1_3_4_54_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00705-021-05162-3"},{"key":"e_1_3_4_55_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1005421"},{"key":"e_1_3_4_56_2","doi-asserted-by":"crossref","unstructured":"N. Hasegawa Evolutionarily diverse origins of honey bee deformed wing viruses National Library of Medicine Bioproject PRJDB14940 https:\/\/www.ncbi.nlm.nih.gov\/bioproject\/923870. 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