{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,27]],"date-time":"2026-03-27T04:04:58Z","timestamp":1774584298891,"version":"3.50.1"},"reference-count":122,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2024,7,15]],"date-time":"2024-07-15T00:00:00Z","timestamp":1721001600000},"content-version":"vor","delay-in-days":196,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100008530","name":"Fundo Europeu de Desenvolvimento Regional","doi-asserted-by":"publisher","award":["POCI-01-0145-FEDER-029871"],"award-info":[{"award-number":["POCI-01-0145-FEDER-029871"]}],"id":[{"id":"10.13039\/501100008530","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007794","name":"Stiftelsen Oscar och Lili Lamms Minne","doi-asserted-by":"publisher","award":["FO2020-0011"],"award-info":[{"award-number":["FO2020-0011"]}],"id":[{"id":"10.13039\/100007794","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["LA\/P\/0007\/2021 SFRH\/BD\/143627\/2019 UIDB\/00690\/2020 UIDP\/00690\/2020"],"award-info":[{"award-number":["LA\/P\/0007\/2021 SFRH\/BD\/143627\/2019 UIDB\/00690\/2020 UIDP\/00690\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001862","name":"Svenska Forskningsr\u00e5det Formas","doi-asserted-by":"publisher","award":["2017-00623 2018-01142 2022-01462"],"award-info":[{"award-number":["2017-00623 2018-01142 2022-01462"]}],"id":[{"id":"10.13039\/501100001862","id-type":"DOI","asserted-by":"publisher"}]},{"name":"National Programme for the Beekeeping Sector","award":["2021-1836"],"award-info":[{"award-number":["2021-1836"]}]},{"DOI":"10.13039\/501100004359","name":"Vetenskapsr\u00e5det","doi-asserted-by":"publisher","award":["2017-03963 2018-04772"],"award-info":[{"award-number":["2017-03963 2018-04772"]}],"id":[{"id":"10.13039\/501100004359","id-type":"DOI","asserted-by":"publisher"}]},{"name":"National Programme for the Beekeeping Sector","award":["2020-1819-2 2021-279"],"award-info":[{"award-number":["2020-1819-2 2021-279"]}]},{"DOI":"10.13039\/501100008530","name":"Fundo Europeu de Desenvolvimento Regional","doi-asserted-by":"publisher","award":["POCI-01-0145-FEDER-029871"],"award-info":[{"award-number":["POCI-01-0145-FEDER-029871"]}],"id":[{"id":"10.13039\/501100008530","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007794","name":"Stiftelsen Oscar och Lili Lamms Minne","doi-asserted-by":"publisher","award":["FO2020-0011"],"award-info":[{"award-number":["FO2020-0011"]}],"id":[{"id":"10.13039\/100007794","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["LA\/P\/0007\/2021 SFRH\/BD\/143627\/2019 UIDB\/00690\/2020 UIDP\/00690\/2020"],"award-info":[{"award-number":["LA\/P\/0007\/2021 SFRH\/BD\/143627\/2019 UIDB\/00690\/2020 UIDP\/00690\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001862","name":"Svenska Forskningsr\u00e5det Formas","doi-asserted-by":"publisher","award":["2017-00623 2018-01142 2022-01462"],"award-info":[{"award-number":["2017-00623 2018-01142 2022-01462"]}],"id":[{"id":"10.13039\/501100001862","id-type":"DOI","asserted-by":"publisher"}]},{"name":"National Programme for the Beekeeping Sector","award":["2021-1836"],"award-info":[{"award-number":["2021-1836"]}]},{"DOI":"10.13039\/501100004359","name":"Vetenskapsr\u00e5det","doi-asserted-by":"publisher","award":["2017-03963 2018-04772"],"award-info":[{"award-number":["2017-03963 2018-04772"]}],"id":[{"id":"10.13039\/501100004359","id-type":"DOI","asserted-by":"publisher"}]},{"name":"National Programme for the Beekeeping Sector","award":["2020-1819-2 2021-279"],"award-info":[{"award-number":["2020-1819-2 2021-279"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,8,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Deformed wing virus (DWV) is a honey bee virus, whose emergence from relative obscurity is driven by the recent host-switch, adaptation, and global dispersal of the ectoparasitic mite Varroa destructor (a highly efficient vector of DWV) to reproduction on honey bees (Apis mellifera). Our study examines how varroa affects the continuing evolution of DWV, using the Azores archipelago, where varroa is present on only three out of the eight Islands, as a natural experimental system for comparing different evolutionary conditions and trajectories. We combined qPCR of 494 honey bee colonies sampled across the archipelago with amplicon deep sequencing to reveal how the DWV genetic landscape is altered by varroa. Two of the varroa-free Islands were also free of DWV, while a further two Islands were intriguingly dominated by the rare DWV-C major variant. The other four Islands, including the three varroa-infested Islands, were dominated by the common DWV-A and DWV-B variants. The varroa-infested Islands had, as expected, an elevated DWV prevalence relative to the uninfested Islands, but not elevated DWV loads, due the relatively high prevalence and loads of DWV-C on the varroa-free Islands. This establishes the Azores as a stable refuge for DWV-C and provides the most convincing evidence to date that at least some major strains of DWV may be capable of not just surviving, but actually thriving in honey bees in the absence of varroa-mediated transmission. We did not detect any change in DWV genetic diversity associated with island varroa status but did find a positive association of DWV diversity with virus load, irrespective of island varroa status.<\/jats:p>","DOI":"10.1093\/ve\/veae053","type":"journal-article","created":{"date-parts":[[2024,7,12]],"date-time":"2024-07-12T20:48:22Z","timestamp":1720817302000},"source":"Crossref","is-referenced-by-count":11,"title":["Origins, diversity, and adaptive evolution of DWV in the honey bees of the Azores: the impact of the invasive mite <i>Varroa destructor<\/i>"],"prefix":"10.1093","volume":"10","author":[{"given":"Ana R","family":"Lopes","sequence":"first","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia , Bragan\u00e7a 5300-253, Portugal"},{"name":"Laborat\u00f3rio Associado para a Sustentabilidade e Tecnologia em Regi\u00f5es de Montanha (SusTEC), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia , Bragan\u00e7a 5300-253, Portugal"},{"name":"REQUIMTE-LAQV, Faculdade de Farm\u00e1cia, Universidade do Porto , Rua de Jorge Viterbo Ferreira, 228, Porto 4050-313, Portugal"}]},{"given":"Matthew","family":"Low","sequence":"additional","affiliation":[{"name":"Department of Ecology, Swedish University of Agricultural Sciences , Uppsala 756-51, Sweden"}]},{"given":"Raquel","family":"Mart\u00edn-Hern\u00e1ndez","sequence":"additional","affiliation":[{"name":"Centro de Investigaci\u00f3n Ap\u00edcola y Agroambiental (CIAPA), IRIAF. Instituto Regional de Investigaci\u00f3n y Desarrollo Agroalimentario y Forestal , Marchamalo 19180, Spain"},{"name":"Instituto de Recursos Humanos para la Ciencia y la Tecnolog\u00eda (INCRECYT-FEDER), Fundaci\u00f3n Parque Cient\u00edfico y Tecnol\u00f3gico de Castilla\u2014La Mancha , Albacete 02006, Spain"}]},{"given":"M Alice","family":"Pinto","sequence":"additional","affiliation":[{"name":"Centro de Investiga\u00e7\u00e3o de Montanha (CIMO), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia , Bragan\u00e7a 5300-253, Portugal"},{"name":"Laborat\u00f3rio Associado para a Sustentabilidade e Tecnologia em Regi\u00f5es de Montanha (SusTEC), Instituto Polit\u00e9cnico de Bragan\u00e7a, Campus de Santa Apol\u00f3nia , Bragan\u00e7a 5300-253, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0335-0386","authenticated-orcid":false,"given":"Joachim R","family":"De Miranda","sequence":"additional","affiliation":[{"name":"Department of Ecology, Swedish University of Agricultural Sciences , Uppsala 756-51, Sweden"}]}],"member":"286","published-online":{"date-parts":[[2024,7,15]]},"reference":[{"key":"2024081308093569000_R1","doi-asserted-by":"publisher","first-page":"W537","DOI":"10.1093\/nar\/gky379","article-title":"The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update","volume":"46","author":"Afgan","year":"2018","journal-title":"Nucleic Acids Research"},{"key":"2024081308093569000_R2","article-title":"A fatal error in determining a race of honeybee","volume":"5","author":"Alpatov","year":"1976","journal-title":"Prirpda"},{"key":"2024081308093569000_R3","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1023\/A:1006456720416","article-title":"Varroa jacobsoni (Acari: Varroidae) is more than one species","volume":"24","author":"Anderson","year":"2000","journal-title":"Exp Appl Acarol"},{"key":"2024081308093569000_R4","article-title":"Apia\u00e7or, Boletim de Informa\u00e7\u00e3o Ap\u00edcola n\u00ba1","author":"Anonymous","year":"1987"},{"key":"2024081308093569000_R5","first-page":"257","article-title":"T\u00e4nap\u00e4eva mesindus","author":"Asten","year":"2019"},{"key":"2024081308093569000_R6","doi-asserted-by":"crossref","DOI":"10.5424\/sjar\/2019173-13991","article-title":"Does pollen diversity influence honey bee colony health?","volume":"17","author":"Barroso-Ar\u00e9valo","year":"2019","journal-title":"Spanish J Agric Res"},{"key":"2024081308093569000_R7","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1016\/j.cels.2018.05.012","article-title":"Community-driven data analysis training for biology","volume":"6","author":"Batut","year":"2018","journal-title":"Cell Systems"},{"key":"2024081308093569000_R8","doi-asserted-by":"crossref","DOI":"10.3390\/insects11040239","article-title":"Diversity and global distribution of viruses of the western honey bee, Apis mellifera","volume":"11","author":"Beaurepaire","year":"2020","journal-title":"Insects"},{"key":"2024081308093569000_R9","first-page":"7","article-title":"Varroosis","volume":"4","author":"Belchior","year":"1996","journal-title":"Apicultor"},{"key":"2024081308093569000_R10","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1111\/mec.14840","article-title":"Quantitative and qualitative assessment of pollen DNA metabarcoding using constructed species mixtures","volume":"28","author":"Bell","year":"2019","journal-title":"Mol Ecol"},{"key":"2024081308093569000_R11","doi-asserted-by":"crossref","first-page":"6345","DOI":"10.1111\/mec.16689","article-title":"Plants, pollinators and their interactions under global ecological change: the role of pollen DNA metabarcoding","volume":"32","author":"Bell","year":"2023","journal-title":"Mol Ecol"},{"key":"2024081308093569000_R12","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1080\/0005772X.2020.1800330","article-title":"World honey bee health: the global distribution of western honey bee (Apis mellifera L.) pests and pathogens","volume":"98","author":"Boncristiani","year":"2021","journal-title":"Bee World"},{"key":"2024081308093569000_R13","doi-asserted-by":"crossref","first-page":"1250","DOI":"10.1038\/s41559-017-0246-z","article-title":"Ecological and evolutionary approaches to managing honeybee disease","volume":"1","author":"Brosi","year":"2017","journal-title":"Nat Ecol Evol"},{"key":"2024081308093569000_R14","doi-asserted-by":"crossref","DOI":"10.1098\/rsbl.2022.0589","article-title":"The final frontier: ecological and evolutionary dynamics of a global parasite invasion","volume":"19","author":"Chapman","year":"2023","journal-title":"Biol Lett"},{"key":"2024081308093569000_R15","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1008922","article-title":"Invasive alien species and disease risk: an open challenge in public and animal health","volume":"16","author":"Chinchio","year":"2020","journal-title":"Plos Pathogens"},{"key":"2024081308093569000_R16","first-page":"39","article-title":"The health status of Irish honeybee colonies in 2006","volume":"52","author":"Coffey","year":"2013","journal-title":"Ir J Agric Food Res"},{"key":"2024081308093569000_R17","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1051\/apido:19970605","article-title":"Fluvalinate resistance of Varroa jacobsoni oudemans (Acari: Varroidae) in Mediterranean apiaries of France","volume":"28","author":"Colin","year":"1997","journal-title":"Apidologie"},{"key":"2024081308093569000_R18","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1080\/0005772X.1978.11097718","article-title":"The varroa mite","volume":"59","author":"Crane","year":"1978","journal-title":"Bee World"},{"key":"2024081308093569000_R19","doi-asserted-by":"crossref","DOI":"10.1038\/srep41045","article-title":"Evidence for positive selection and recombination hotspots in Deformed wing virus (DWV)","volume":"7","author":"Dalmon","year":"2017","journal-title":"Sci Rep"},{"key":"2024081308093569000_R20","doi-asserted-by":"crossref","DOI":"10.1128\/jvi.01149-23","article-title":"Virus replication in the honey bee parasite, Varroa destructor","volume":"97","author":"Damayo","year":"2023","journal-title":"J Virol"},{"key":"2024081308093569000_R21","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1146\/annurev.en.27.010182.001305","article-title":"Mite pests of honey bees","volume":"27","author":"De Jong","year":"1982","journal-title":"Annu Rev Entomol"},{"key":"2024081308093569000_R22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3896\/IBRA.1.52.4.22","article-title":"Standard methods for virus research in Apis mellifera","volume":"52","author":"De Miranda","year":"2013","journal-title":"J Apic Res"},{"key":"2024081308093569000_R23","doi-asserted-by":"crossref","DOI":"10.1186\/s12985-022-01740-2","article-title":"Cold case: the disappearance of Egypt bee virus, a fourth distinct master strain of deformed wing virus linked to honeybee mortality in 1970\u2019s Egypt","volume":"19","author":"De Miranda","year":"2022","journal-title":"Virol J"},{"key":"2024081308093569000_R24","doi-asserted-by":"crossref","first-page":"S48","DOI":"10.1016\/j.jip.2009.06.012","article-title":"Deformed wing virus","volume":"103","author":"De Miranda","year":"2010","journal-title":"J Invertebr Pathol"},{"key":"2024081308093569000_R25","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1099\/jgv.0.001206","article-title":"Occurrence of deformed wing virus variants in the stingless bee melipona subnitida and honey bee Apis mellifera populations in Brazil","volume":"100","author":"De Souza","year":"2019","journal-title":"J Gen Virol"},{"key":"2024081308093569000_R26","first-page":"16","article-title":"25 Jahre Varroa in der Schweiz","volume-title":"Schweizerische Bienen-Zeitung","author":"Diller","year":"2009"},{"key":"2024081308093569000_R27","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1146\/annurev-virology-101416-041718","article-title":"Mechanisms and concepts in RNA virus population dynamics and evolution","volume":"5","author":"Dolan","year":"2018","journal-title":"Annu Rev Virol"},{"key":"2024081308093569000_R28","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1008271","article-title":"Viral quasispecies","volume":"15","author":"Domingo","year":"2019","journal-title":"PLoS Genet"},{"key":"2024081308093569000_R29","doi-asserted-by":"crossref","DOI":"10.1098\/rsos.231529","article-title":"Shift in virus composition in honeybees Apis mellifera following worldwide invasion by the parasitic mite and virus vector Varroa destructor","volume":"11","author":"Doublet","year":"2024","journal-title":"Royal Soc Open Sci"},{"key":"2024081308093569000_R30","article-title":"Commission Implementing Decision (EU) 2019\/1895 of 7 November 2019 recognising several Islands in Portugal as free from varroosis and amending the Annex to Implementing Decision 2013\/503\/EU (notified under document C(2019) 7905) (Text with EEA relevance)","volume-title":"Brussels: Official Journal of the European Union","author":"European Commission","year":"2019"},{"key":"2024081308093569000_R31","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1007\/s13592-019-00720-w","article-title":"Historical and contemporaneous human-mediated processes left a strong genetic signature on honey bee populations from the Macaronesian archipelago of the Azores","volume":"51","author":"Ferreira","year":"2020","journal-title":"Apidologie"},{"key":"2024081308093569000_R32","doi-asserted-by":"crossref","DOI":"10.1186\/1743-422X-3-16","article-title":"Localization of deformed wing virus infection in queen and drone Apis mellifera L","volume":"3","author":"Fievet","year":"2006","journal-title":"Virol J"},{"key":"2024081308093569000_R33","article-title":"Varroa infestation in \u00c5land Islands, Finland","author":"Finnish Food Authority","year":"2021"},{"key":"2024081308093569000_R34","doi-asserted-by":"crossref","first-page":"136","DOI":"10.3896\/IBRA.1.51.1.17","article-title":"Adult honey bees (Apis mellifera) with deformed wings discovered in confirmed varroa-free colonies","volume":"51","author":"Forsgren","year":"2012","journal-title":"J Apic Res"},{"key":"2024081308093569000_R35","first-page":"29","article-title":"Current situation of varroatosis in Italy","author":"Frilli","year":"1988"},{"key":"2024081308093569000_R36","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1038\/nature12977","article-title":"Disease associations between honeybees and bumblebees as a threat to wild pollinators","volume":"506","author":"F\u00fcrst","year":"2014","journal-title":"Nature"},{"key":"2024081308093569000_R37","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-023-49688-9","article-title":"Reproduction of Varroa destructor depends on well-timed host cell recapping and seasonal patterns","volume":"13","author":"Gabel","year":"2023","journal-title":"Sci Rep"},{"key":"2024081308093569000_R38","doi-asserted-by":"crossref","DOI":"10.1128\/JVI.01786-20","article-title":"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","volume":"95","author":"Gisder","year":"2021","journal-title":"J Virol"},{"key":"2024081308093569000_R39","doi-asserted-by":"crossref","first-page":"4612","DOI":"10.1111\/1462-2920.14481","article-title":"In vivo evolution of viral virulence: switching of deformed wing virus between hosts results in virulence changes and sequence shifts","volume":"20","author":"Gisder","year":"2018","journal-title":"Environ Microbiol"},{"key":"2024081308093569000_R40","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0128122","article-title":"Deconstructing the polymerase chain reaction: understanding and correcting bias associated with primer degeneracies and primer-template mismatches","volume":"10","author":"Green","year":"2015","journal-title":"PloS One"},{"key":"2024081308093569000_R41","doi-asserted-by":"crossref","DOI":"10.3390\/v13060969","article-title":"Ten 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","volume":"13","author":"Grindrod","year":"2021","journal-title":"Viruses"},{"key":"2024081308093569000_R42","doi-asserted-by":"crossref","DOI":"10.1007\/s13592-022-00977-8","article-title":"Varroa resistance in Apis cerana: a review","volume":"54","author":"Grindrod","year":"2023","journal-title":"Apidologie"},{"key":"2024081308093569000_R43","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":"2024081308093569000_R44","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1038\/s41564-018-0296-2","article-title":"Tracking virus outbreaks in the twenty-first century","volume":"4","author":"Grubaugh","year":"2019","journal-title":"Nat Microbiol"},{"key":"2024081308093569000_R45","article-title":"Life-history stage determines the diet of ectoparasitic mites on their honey bee hosts","volume":"15","author":"Han","year":"2024","journal-title":"Nat Commun"},{"key":"2024081308093569000_R46","article-title":"Varroa fundet i Danmark","volume":"118","author":"Hansen","year":"1984","journal-title":"Tidsskrift for Biavl"},{"key":"2024081308093569000_R47","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.2301258120","article-title":"Evolutionarily diverse origins of deformed wing viruses in western honey bees","volume":"120","author":"Hasegawa","year":"2023","journal-title":"Proc Natl Acad Sci"},{"key":"2024081308093569000_R48","article-title":"16S Microbial Analysis with mothur (extended) (Galaxy Training Materials","author":"Hiltemann","year":"2023"},{"key":"2024081308093569000_R49","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1010752","article-title":"Galaxy training: a powerful framework for teaching!","volume":"19","author":"Hiltemann","year":"2023","journal-title":"PLoS Comput Biol"},{"key":"2024081308093569000_R50","doi-asserted-by":"crossref","DOI":"10.13102\/sociobiology.v68i1.5851","article-title":"Honey bee colony losses: why are honey bees disappearing?","volume":"68","author":"Hristov","year":"2021","journal-title":"Sociobiology"},{"key":"2024081308093569000_R51","doi-asserted-by":"crossref","DOI":"10.1016\/j.scitotenv.2019.135044","article-title":"Plant-insect vector-virus interactions under environmental change","volume":"701","author":"Islam","year":"2020","journal-title":"Sci Total Environ"},{"key":"2024081308093569000_R52","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1093\/bioinformatics\/btn129","article-title":"Adegenet: a R package for the multivariate analysis of genetic markers","volume":"24","author":"Jombart","year":"2008","journal-title":"Bioinformatics"},{"key":"2024081308093569000_R53","doi-asserted-by":"publisher","first-page":"94","DOI":"10.1186\/1471-2156-11-94","article-title":"Discriminant analysis of principal components: a new method for the analysis of genetically structured populations","volume":"11","author":"Jombart","year":"2010","journal-title":"BMC GenetBMC Genetics"},{"key":"2024081308093569000_R54","first-page":"85","article-title":"Varroatose in Finnland","volume":"16","author":"Kauko","year":"1992","journal-title":"Ann Univ Mariae Curie-Sklodowska Sect"},{"key":"2024081308093569000_R55","doi-asserted-by":"crossref","DOI":"10.3390\/v11050426","article-title":"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","volume":"11","author":"Kevill","year":"2019","journal-title":"Viruses"},{"key":"2024081308093569000_R56","doi-asserted-by":"crossref","DOI":"10.3390\/v9110314","article-title":"ABC assay: method development and application to quantify the role of three DWV master variants in overwinter colony losses of European honey bees","volume":"9","author":"Kevill","year":"2017","journal-title":"Viruses-Basel"},{"key":"2024081308093569000_R57","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1016\/j.ympev.2007.09.005","article-title":"Utility of DNA viruses for studying human host history: case study of JC virus","volume":"46","author":"Kitchen","year":"2008","journal-title":"Mol Phylogen Evol"},{"key":"2024081308093569000_R58","doi-asserted-by":"publisher","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Molecular Biology and Evolution"},{"key":"2024081308093569000_R59","doi-asserted-by":"crossref","first-page":"4998","DOI":"10.1128\/JVI.80.10.4998-5009.2006","article-title":"Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.)","volume":"80","author":"Lanzi","year":"2006","journal-title":"J Virol"},{"key":"2024081308093569000_R60","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-022-12888-w","article-title":"Viral communities in the parasite Varroa destructor and in colonies of their honey bee host (Apis mellifera) in New Zealand","volume":"12","author":"Lester","year":"2022","journal-title":"Sci Rep"},{"key":"2024081308093569000_R61","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0180910","article-title":"Persistence of subclinical deformed wing virus infections in honeybees following Varroa mite removal and a bee population turnover","volume":"12","author":"Locke","year":"2017","journal-title":"PLoS ONE"},{"key":"2024081308093569000_R62","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1012337","article-title":"Varroa destructor shapes the unique viral landscapes of the honey bee populations of the Azores archipelago","volume":"20","author":"Lopes","year":"2024","journal-title":"PloS Pathogens"},{"key":"2024081308093569000_R63","article-title":"Colonisation patterns of Nosema ceranae in the Azores archipelago","volume":"9","author":"Lopes","year":"2022","journal-title":"Vet Sci"},{"key":"2024081308093569000_R64","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1080\/00218839.2023.2172835","article-title":"First detection of Nosema ceranae in honey bees (Apis mellifera L.) of the Macaronesian archipelago of Madeira","volume":"62","author":"Lopes","year":"2023","journal-title":"J Apic Res"},{"key":"2024081308093569000_R65","doi-asserted-by":"crossref","first-page":"1306","DOI":"10.1111\/ele.13323","article-title":"Knock-on community impacts of a novel vector: spillover of emerging DWV-B from Varroa-infested honeybees to wild bumblebees","volume":"22","author":"Manley","year":"2019","journal-title":"Ecol Lett"},{"key":"2024081308093569000_R66","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1146\/annurev-virology-092818-015700","article-title":"Deformed wing virus in honeybees and other insects","volume":"6","author":"Martin","year":"2019","journal-title":"Annu Rev Virol"},{"key":"2024081308093569000_R67","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":"2024081308093569000_R68","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1111\/1365-2656.12345","article-title":"A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees","volume":"84","author":"McMahon","year":"2015","journal-title":"J Anim Ecol"},{"key":"2024081308093569000_R69","doi-asserted-by":"crossref","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"},{"key":"2024081308093569000_R70","first-page":"565","article-title":"Ouessant colonis\u00e9e par Varroa destructor!","volume":"306","author":"M\u00e9nage","year":"2021","journal-title":"La Sant\u00e9 de l\u2019Abeille"},{"key":"2024081308093569000_R71","article-title":"Orden de 28 de febrero de 1986 por la que se declara la existencia de Varroasis en Espa\u00f1a y se dictan normas de lucha","volume":"58","author":"Ministerio de agricultura, pesca y alimentaci\u00f3n","year":"1986","journal-title":"Bolet\u00edn Oficial Del Estado Num"},{"key":"2024081308093569000_R72","article-title":"More than sixty years living with Varroa destructor: a review of acaricide resistance","volume":"24","author":"Mitton","year":"2022","journal-title":"Int J Pest Manag"},{"key":"2024081308093569000_R73","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":"M\u00f6ckel","year":"2011","journal-title":"J Gen Virol"},{"key":"2024081308093569000_R74","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1004323","article-title":"On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor","volume":"10","author":"Mondet","year":"2014","journal-title":"Plos Pathogens"},{"key":"2024081308093569000_R75","doi-asserted-by":"crossref","DOI":"10.1038\/srep25444","article-title":"Specific cues associated with honey bee social defence against Varroa destructor infested brood","volume":"6","author":"Mondet","year":"2016","journal-title":"Sci Rep"},{"key":"2024081308093569000_R76","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1099\/vir.0.025965-0","article-title":"Recombinants between deformed wing virus and varroa destructor virus-1 may prevail in varroa destructor-infested honeybee colonies","volume":"92","author":"Moore","year":"2011","journal-title":"J Gen Virol"},{"key":"2024081308093569000_R77","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":"2024081308093569000_R78","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-017-05596-3","article-title":"The virulent, emerging genotype B of Deformed wing virus is closely linked to overwinter honeybee worker loss","volume":"7","author":"Natsopoulou","year":"2017","journal-title":"Sci Rep"},{"key":"2024081308093569000_R79","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1126\/science.abg2297","article-title":"Tracking the UK SARS-CoV-2 outbreak","volume":"371","author":"Nelson","year":"2021","journal-title":"Science"},{"key":"2024081308093569000_R80","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/j.pt.2012.06.004","article-title":"Varroa invasion and virus adaptation","volume":"28","author":"Neumann","year":"2012","journal-title":"Trends Parasitol"},{"key":"2024081308093569000_R81","doi-asserted-by":"crossref","DOI":"10.3389\/fmicb.2020.00620","article-title":"Accumulation and competition amongst deformed wing virus genotypes in na\u00efve Australian honeybees provides insight into the increasing global prevalence of genotype B","volume":"11","author":"Norton","year":"2020","journal-title":"Front Microbiol"},{"key":"2024081308093569000_R82","doi-asserted-by":"crossref","first-page":"2254","DOI":"10.1111\/1365-2656.13493","article-title":"Adaptation to vector-based transmission in a honeybee virus","volume":"90","author":"Norton","year":"2021","journal-title":"J Anim Ecol"},{"key":"2024081308093569000_R83","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-021-88592-y","article-title":"Reproductive success of the parasitic mite (Varroa destructor) is lower in honeybee colonies that target infested cells with recapping","volume":"11","author":"Oddie","year":"2021","journal-title":"Sci Rep"},{"key":"2024081308093569000_R84","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1080\/0005772X.2021.1882783","article-title":"Insights from Norway: using natural adaptation to breed varroa-resistant honey bees","volume":"98","author":"Oddie","year":"2021","journal-title":"Bee World"},{"key":"2024081308093569000_R85","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-018-26001-7","article-title":"Rapid parallel evolution overcomes global honey bee parasite","volume":"8","author":"Oddie","year":"2018","journal-title":"Sci Rep"},{"key":"2024081308093569000_R86","article-title":"Vegan: Community Ecology Package. R package version 2.6-4","author":"Oksanen","year":"2022"},{"key":"2024081308093569000_R87","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":"2024081308093569000_R88","first-page":"95","article-title":"The mite marches on: Varroa jacobsoni found in the UK","volume":"73","author":"Paxton","year":"1992","journal-title":"Bee World"},{"key":"2024081308093569000_R89","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.ijppaw.2022.04.013","article-title":"Epidemiology of a major honey bee pathogen, deformed wing virus: potential worldwide replacement of genotype A by genotype B","volume":"18","author":"Paxton","year":"2022","journal-title":"Int J Parasitol Parasites Wildl"},{"key":"2024081308093569000_R90","article-title":"JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling","author":"Plummer","year":"2003"},{"key":"2024081308093569000_R91","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-12-38","article-title":"Removing Noise From Pyrosequenced Amplicons","volume":"12","author":"Quince","year":"2011","journal-title":"BMC Bioinformatics"},{"key":"2024081308093569000_R92","doi-asserted-by":"crossref","DOI":"10.1098\/rspb.2023.1965","article-title":"Signatures of adaptive decreased virulence of deformed wing virus in an isolated population of wild honeybees (Apis mellifera)","volume":"290","author":"Ray","year":"2023","journal-title":"Proc R Soc B"},{"key":"2024081308093569000_R93","article-title":"R: A language and environment for statistical computing","volume-title":"R Foundation for Statistical Computing, Vienna, Austria","author":"R Core Team","year":"2022"},{"key":"2024081308093569000_R94","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-017-07290-w","article-title":"Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses","volume":"7","author":"Roberts","year":"2017","journal-title":"Sci Rep"},{"key":"2024081308093569000_R95","doi-asserted-by":"crossref","first-page":"2379","DOI":"10.1111\/mec.13185","article-title":"Multiple host shifts by the emerging honeybee parasite, Varroa jacobsoni","volume":"24","author":"Roberts","year":"2015","journal-title":"Mol Ecol"},{"key":"2024081308093569000_R96","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.3000502","article-title":"Dynamic evolution in the key honey bee pathogen deformed wing virus: novel insights into virulence and competition using reverse genetics","volume":"17","author":"Ryabov","year":"2019","journal-title":"PLoS Biol"},{"key":"2024081308093569000_R97","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1004230","article-title":"A virulent strain of Deformed Wing Virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission","volume":"10","author":"Ryabov","year":"2014","journal-title":"Plos Pathogens"},{"key":"2024081308093569000_R98","doi-asserted-by":"publisher","first-page":"7537","DOI":"10.1128\/AEM.01541-09","article-title":"Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities","volume":"75","author":"Schloss","year":"2009","journal-title":"Appl Environ Microbiol"},{"key":"2024081308093569000_R99","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0098599","article-title":"Honey bee Apis mellifera parasites in the absence of Nosema ceranae fungi and Varroa destructor mites","volume":"9","author":"Shutler","year":"2014","journal-title":"PLoS One"},{"key":"2024081308093569000_R100","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1080\/00218839.2021.1902679","article-title":"Honey bee pathogens and parasites in Swedish apiaries: a baseline study","volume":"60","author":"Silva de Oliveira","year":"2021","journal-title":"J Apic Res"},{"key":"2024081308093569000_R101","doi-asserted-by":"crossref","DOI":"10.3389\/fevo.2022.1027297","article-title":"Spatial analysis of Varroa destructor and the relationship with surrounding landscape types in Southern Ontario","volume":"10","author":"Sobkowich","year":"2022","journal-title":"Front Ecol Evol"},{"key":"2024081308093569000_R102","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1111\/1365-2435.12011","article-title":"Invading with biological weapons: the importance of disease-mediated invasions","volume":"26","author":"Strauss","year":"2012","journal-title":"Funct Ecol"},{"key":"2024081308093569000_R103","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1111\/j.1365-2656.2004.00776.x","article-title":"The dynamics of virus epidemics in Varroa-infested honey bee colonies","volume":"73","author":"Sumpter","year":"2004","journal-title":"J Anim Ecol"},{"key":"2024081308093569000_R104","first-page":"678","article-title":"Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C- content biases","volume":"9","author":"Tamura","year":"1992","journal-title":"Mol Biol Evol"},{"key":"2024081308093569000_R105","doi-asserted-by":"crossref","DOI":"10.1098\/rsos.200480","article-title":"Experimental infection of bumblebees with honeybee-associated viruses: no direct fitness costs but potential future threats to novel wild bee hosts","volume":"7","author":"Tehel","year":"2020","journal-title":"Royal Soc Open Sci"},{"key":"2024081308093569000_R106","doi-asserted-by":"crossref","DOI":"10.3390\/v11020114","article-title":"The two prevalent genotypes of an emerging infectious disease, deformed wing virus, cause equally low pupal mortality and equally high wing deformities in host honey bees","volume":"11","author":"Tehel","year":"2019","journal-title":"Viruses"},{"key":"2024081308093569000_R107","doi-asserted-by":"crossref","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"},{"key":"2024081308093569000_R108","doi-asserted-by":"crossref","first-page":"4673","DOI":"10.1093\/nar\/22.22.4673","article-title":"CLUSTAL-W - improving the sensitibity of progressive multiple sequence alignment through sequence weighting, posistion-specific gap penalties and weigh matrix choice","volume":"22","author":"Thompson","year":"1994","journal-title":"Nucleic Acids Res"},{"key":"2024081308093569000_R109","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1051\/apido:2007021","article-title":"Incidence and molecular characterization of viruses found in dying New Zealand honey bee (Apis mellifera) colonies infested with Varroa destructor","volume":"38","author":"Todd","year":"2007","journal-title":"Apidologie"},{"key":"2024081308093569000_R110","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1016\/j.pt.2020.04.004","article-title":"Varroa destructor: a complex parasite, crippling honey bees worldwide","volume":"36","author":"Traynor","year":"2020","journal-title":"Trends Parasitol"},{"key":"2024081308093569000_R111","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1009175","article-title":"Stability of SARS-CoV-2 phylogenies","volume":"16","author":"Turakhia","year":"2020","journal-title":"Plos Genetics"},{"key":"2024081308093569000_R112","article-title":"Sequence recombination and conservation of Varroa destructor virus-1 and deformed wing virus in field collected honey bees (Apis mellifera)","volume":"8","author":"Wang","year":"2013","journal-title":"PloS One"},{"key":"2024081308093569000_R113","first-page":"341","article-title":"Varroa mite spread in the United States","volume":"124","author":"Wenner","year":"1996","journal-title":"Bee Culture"},{"key":"2024081308093569000_R114","volume-title":"Island Biogeography: Ecology, Evolution, and Conservation","author":"Whittaker","year":"2007"},{"key":"2024081308093569000_R115","doi-asserted-by":"crossref","DOI":"10.1016\/j.scitotenv.2022.159735","article-title":"Maximising signal-to-noise ratios in environmental DNA-based monitoring","volume":"858","author":"Wilding","year":"2023","journal-title":"Sci Total Environ"},{"key":"2024081308093569000_R116","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1126\/science.aac9976","article-title":"Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites","volume":"351","author":"Wilfert","year":"2016","journal-title":"Science"},{"key":"2024081308093569000_R117","doi-asserted-by":"crossref","DOI":"10.1093\/femsre\/fuaa070","article-title":"Deformed wing virus: using reverse genetics to tackle unanswered questions about the most important viral pathogen of honey bees","volume":"45","author":"Woodford","year":"2021","journal-title":"FEMS Microbiol Rev"},{"key":"2024081308093569000_R118","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.mimet.2009.03.001","article-title":"Quantitative effects of position and type of single mismatch on single base primer extension","volume":"77","author":"Wu","year":"2009","journal-title":"J Microbiol Methods"},{"key":"2024081308093569000_R119","doi-asserted-by":"crossref","DOI":"10.1186\/s12866-015-0450-4","article-title":"Phasing amplicon sequencing on Illumina Miseq for robust environmental microbial community analysis","volume":"15","author":"Wu","year":"2015","journal-title":"BMC Microbiol"},{"key":"2024081308093569000_R120","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-020-62673-w","article-title":"The honeybee (Apis mellifera) developmental state shapes the genetic composition of the deformed wing virus-A quasispecies during serial transmission","volume":"10","author":"Ya\u00f1ez","year":"2020","journal-title":"Sci Rep"},{"key":"2024081308093569000_R121","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s13592-011-0088-7","article-title":"Deformed wing virus and drone mating flights in the honey bee (Apis mellifera): implications for sexual transmission of a major honey bee virus","volume":"43","author":"Ya\u00f1ez","year":"2012","journal-title":"Apidologie"},{"key":"2024081308093569000_R122","doi-asserted-by":"crossref","DOI":"10.3389\/fmicb.2020.00943","article-title":"Bee viruses: routes of infection in hymenoptera","volume":"11","author":"Ya\u00f1ez","year":"2020","journal-title":"Front Microbiol"}],"container-title":["Virus Evolution"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/ve\/advance-article-pdf\/doi\/10.1093\/ve\/veae053\/58546211\/veae053.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ve\/article-pdf\/10\/1\/veae053\/58803230\/veae053.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ve\/article-pdf\/10\/1\/veae053\/58803230\/veae053.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,13]],"date-time":"2024-08-13T11:01:34Z","timestamp":1723546894000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ve\/article\/doi\/10.1093\/ve\/veae053\/7713834"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024]]},"references-count":122,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2024,8,7]]}},"URL":"https:\/\/doi.org\/10.1093\/ve\/veae053","relation":{},"ISSN":["2057-1577"],"issn-type":[{"value":"2057-1577","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024]]},"published":{"date-parts":[[2024]]},"article-number":"veae053"}}