{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T19:50:57Z","timestamp":1790970657847,"version":"4.1.0"},"reference-count":99,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2026,6,25]],"date-time":"2026-06-25T00:00:00Z","timestamp":1782345600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100022077","name":"Institut National de Recherche pour l\u2019Agriculture, l\u2019Alimentation et l\u2019Environnement","doi-asserted-by":"publisher","award":["VIRVARBEE"],"award-info":[{"award-number":["VIRVARBEE"]}],"id":[{"id":"10.13039\/501100022077","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100022077","name":"Institut National de Recherche pour l\u2019Agriculture, l\u2019Alimentation et l\u2019Environnement","doi-asserted-by":"publisher","award":["VIRVARBEE"],"award-info":[{"award-number":["VIRVARBEE"]}],"id":[{"id":"10.13039\/501100022077","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007545","name":"Agence Fran\u00e7aise de S\u00e9curit\u00e9 Sanitaire de l\u2019Environnement et du Travail","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100007545","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007545","name":"Agence Fran\u00e7aise de S\u00e9curit\u00e9 Sanitaire de l\u2019Environnement et du Travail","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100007545","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>Honey bees are commonly infected with viruses, including deformed wing virus (DWV-A and DWV-B) and sacbrood virus (SBV), which cause morphological symptoms and death in developing bees and primarily asymptomatic infections in adult bees. Co-infections occur regularly in colonies, but they have rarely been studied, especially in adult bees. In this study, we co-inoculated young adult honey bees with DWV by injection (simulating vectored transmission by Varroa) and feeding them with SBV (simulating oral transmission) before reintroducing them in colonies. Through the use of optical counters and regular sampling, we tracked their survival and behaviour, and quantified the dynamics of viral loads in treated bees as well as the expression of eight immune genes involved in honey bee anti-viral immunity. Here, we show that co-inoculations of DWV and SBV synergistically increase the virulence of DWV and conditionally promote the replication of SBV. We also show that SBV may play a role in the replication of DWV in specific contexts. Finally, our results show that immune responses in adult honey bees depend on virus genotype (i.e., DWV), their relative abundance and the pre-existing natural infections before virus injection). Together, these results confirm the existence of deleterious interactions between deformed wing virus and sacbrood virus, impacting honey bee health and colony dynamics.<\/jats:p>","DOI":"10.1371\/journal.ppat.1014290","type":"journal-article","created":{"date-parts":[[2026,6,25]],"date-time":"2026-06-25T17:22:56Z","timestamp":1782408176000},"page":"e1014290","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["Co-inoculation with deformed wing virus and sacbrood virus affects viral and immune dynamics and synergistically increases honey bee mortality"],"prefix":"10.1371","volume":"22","author":[{"ORCID":"https:\/\/orcid.org\/0009-0008-2912-2585","authenticated-orcid":true,"given":"Alice M\u00e9lusine","family":"Durand","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric","family":"Dubois","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne","family":"Bonjour-Dalmon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2026,6,25]]},"reference":[{"issue":"2","key":"ppat.1014290.ref001","doi-asserted-by":"crossref","first-page":"119","DOI":"10.17519\/apiculture.2020.06.35.2.119","article-title":"Ecosystem Services of Honey Bees; Regulating, Provisioning and Cultural Functions","volume":"35","author":"S Aryal","year":"2020","journal-title":"apiculture"},{"issue":"10","key":"ppat.1014290.ref002","doi-asserted-by":"crossref","first-page":"3516","DOI":"10.1111\/gcb.14736","article-title":"Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification","volume":"25","author":"MA Aizen","year":"2019","journal-title":"Glob Chang Biol"},{"issue":"6","key":"ppat.1014290.ref003","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.0050168","article-title":"What\u2019s killing American honey bees?","volume":"5","author":"BP Oldroyd","year":"2007","journal-title":"PLoS Biol"},{"issue":"3","key":"ppat.1014290.ref004","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1080\/00218839.2018.1460911","article-title":"Multi-country loss rates of honey bee colonies during winter 2016\/2017 from the COLOSS survey","volume":"57","author":"R Brodschneider","year":"2018","journal-title":"J Apic Res"},{"issue":"2","key":"ppat.1014290.ref005","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1080\/00218839.2022.2113329","article-title":"Honey bee colony loss rates in 37 countries using the COLOSS survey for winter 2019\u20132020: the combined effects of operation size, migration and queen replacement","volume":"62","author":"A Gray","year":"2023","journal-title":"J Apic Res"},{"issue":"6229","key":"ppat.1014290.ref006","doi-asserted-by":"crossref","first-page":"1255957","DOI":"10.1126\/science.1255957","article-title":"Bee declines driven by combined stress from parasites, pesticides, and lack of flowers","volume":"347","author":"D Goulson","year":"2015","journal-title":"Science"},{"key":"ppat.1014290.ref007","doi-asserted-by":"crossref","DOI":"10.1051\/apido:19950307","volume-title":"Parasites and social insects","author":"P Schmid-Hempel","year":"1995"},{"issue":"7","key":"ppat.1014290.ref008","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":"KS Traynor","year":"2020","journal-title":"Trends Parasitol"},{"issue":"8","key":"ppat.1014290.ref009","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/S0169-5347(99)01613-4","article-title":"Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees","volume":"14","author":"B Oldroyd","year":"1999","journal-title":"Trends Ecol Evol"},{"issue":"1","key":"ppat.1014290.ref010","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1051\/apido:19810103","article-title":"Beobachtungen \u00fcber die Anpassung von Varroa jacobsoni an ihren nat\u00fcrlichen Wirt Apis cerana in Sri Lanka","volume":"12","author":"N Koeniger","year":"1981","journal-title":"Apidologie"},{"key":"ppat.1014290.ref011","unstructured":"Guzman LID, Rinderer TE, Guzman LID, Identification TER, Guzman LID. Identification and comparison of Varroa species infesting honey bees. 1999."},{"issue":"4","key":"ppat.1014290.ref012","first-page":"373","article-title":"Presencia de varroa en Uganda y su conocimiento por parte de la industria ap\u00edcola","volume":"54","author":"P Kasangaki","year":"2015","journal-title":"J Apic Res"},{"key":"ppat.1014290.ref013","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.jip.2017.11.008","article-title":"Evidence of Varroa-mediated deformed wing virus spillover in Hawaii","volume":"151","author":"J Santamaria","year":"2018","journal-title":"J Invertebr Pathol"},{"issue":"5","key":"ppat.1014290.ref014","doi-asserted-by":"crossref","first-page":"20220589","DOI":"10.1098\/rsbl.2022.0589","article-title":"The final frontier: ecological and evolutionary dynamics of a global parasite invasion","volume":"19","author":"NC Chapman","year":"2023","journal-title":"Biol Lett"},{"issue":"1901","key":"ppat.1014290.ref015","first-page":"20190331","article-title":"Haemolymph removal by Varroa mite destabilizes the dynamical interaction between immune effectors and virus in bees, as predicted by Volterra\u2019s model","volume":"286","author":"D Annoscia","year":"2019","journal-title":"Proc Biol Sci"},{"issue":"1","key":"ppat.1014290.ref016","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/s41467-024-44915-x","article-title":"Life-history stage determines the diet of ectoparasitic mites on their honey bee hosts","volume":"15","author":"B Han","year":"2024","journal-title":"Nat Commun"},{"issue":"5","key":"ppat.1014290.ref017","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":"SD Ramsey","year":"2019","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ppat.1014290.ref018","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1099\/vir.0.023853-0","article-title":"Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera","volume":"92","author":"G Di Prisco","year":"2011","journal-title":"J Gen Virol"},{"key":"ppat.1014290.ref019","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":"N M\u00f6ckel","year":"2011","journal-title":"J Gen Virol"},{"issue":"1","key":"ppat.1014290.ref020","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1128\/AEM.06094-11","article-title":"Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control","volume":"78","author":"B Locke","year":"2012","journal-title":"Appl Environ Microbiol"},{"issue":"6086","key":"ppat.1014290.ref021","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":"SJ Martin","year":"2012","journal-title":"Science"},{"issue":"11","key":"ppat.1014290.ref022","first-page":"001687","article-title":"Simulated vector transmission differentially influences dynamics of two viral variants of deformed wing virus in honey bees (Apis mellifera)","volume":"102","author":"AM Ray","year":"2021","journal-title":"J Gen Virol"},{"issue":"10","key":"ppat.1014290.ref023","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":"EV Ryabov","year":"2019","journal-title":"PLoS Biol"},{"key":"ppat.1014290.ref024","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":"J Moore","year":"2011","journal-title":"J Gen Virol"},{"key":"ppat.1014290.ref025","doi-asserted-by":"crossref","first-page":"41045","DOI":"10.1038\/srep41045","article-title":"Evidence for positive selection and recombination hotspots in Deformed wing virus (DWV)","volume":"7","author":"A Dalmon","year":"2017","journal-title":"Sci Rep"},{"key":"ppat.1014290.ref026","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","author":"S Gisder","year":"2021","journal-title":"J Virol"},{"issue":"26","key":"ppat.1014290.ref027","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":"N Hasegawa","year":"2023","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"11","key":"ppat.1014290.ref028","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0113448","article-title":"Infectivity of DWV associated to flower pollen: experimental evidence of a horizontal transmission route","volume":"9","author":"M Mazzei","year":"2014","journal-title":"PLoS One"},{"issue":"7","key":"ppat.1014290.ref029","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":"B Locke","year":"2017","journal-title":"PLoS One"},{"key":"ppat.1014290.ref030","doi-asserted-by":"crossref","first-page":"2329","DOI":"10.1099\/vir.0.83101-0","article-title":"Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera)","volume":"88","author":"C Yue","year":"2007","journal-title":"J Gen Virol"},{"issue":"1","key":"ppat.1014290.ref031","doi-asserted-by":"crossref","first-page":"14310","DOI":"10.1038\/s41598-020-71388-x","article-title":"Heritability estimates of the novel trait \u201csuppressed in ovo virus infection\u201d in honey bees (Apis mellifera)","volume":"10","author":"DC de Graaf","year":"2020","journal-title":"Sci Rep"},{"issue":"2","key":"ppat.1014290.ref032","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1016\/j.jip.2008.02.004","article-title":"Venereal and vertical transmission of deformed wing virus in honeybees (Apis mellifera L.)","volume":"98","author":"JR de Miranda","year":"2008","journal-title":"J Invertebr Pathol"},{"key":"ppat.1014290.ref033","doi-asserted-by":"crossref","DOI":"10.1038\/srep33065","article-title":"Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens","volume":"6","author":"E Amiri","year":"2016","journal-title":"Sci Rep"},{"issue":"11","key":"ppat.1014290.ref034","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0242688","article-title":"Varroa destructor mites vector and transmit pathogenic honey bee viruses acquired from an artificial diet","volume":"15","author":"F Posada-Florez","year":"2020","journal-title":"PLoS One"},{"issue":"1833","key":"ppat.1014290.ref035","first-page":"20160811","article-title":"Elevated virulence of an emerging viral genotype as a driver of honeybee loss","volume":"283","author":"DP McMahon","year":"2016","journal-title":"Proc Biol Sci"},{"key":"ppat.1014290.ref036","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":"S Gisder","year":"2009","journal-title":"J Gen Virol"},{"issue":"12","key":"ppat.1014290.ref037","doi-asserted-by":"crossref","DOI":"10.1128\/jvi.01149-23","article-title":"Virus replication in the honey bee parasite, Varroa destructor","volume":"97","author":"JE Damayo","year":"2023","journal-title":"J Virol"},{"issue":"1833","key":"ppat.1014290.ref038","first-page":"20160811","article-title":"Elevated virulence of an emerging viral genotype as a driver of honeybee loss","volume":"283","author":"DP McMahon","year":"2016","journal-title":"Proc Biol Sci"},{"issue":"1","key":"ppat.1014290.ref039","doi-asserted-by":"crossref","first-page":"5242","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":"ME Natsopoulou","year":"2017","journal-title":"Sci Rep"},{"key":"ppat.1014290.ref040","doi-asserted-by":"crossref","first-page":"620","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":"AM Norton","year":"2020","journal-title":"Front Microbiol"},{"key":"ppat.1014290.ref041","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":"RJ Paxton","year":"2022","journal-title":"Int J Parasitol Parasites Wildl"},{"issue":"1617","key":"ppat.1014290.ref042","first-page":"1517","article-title":"Virus infection causes specific learning deficits in honeybee foragers","volume":"274","author":"J Iqbal","year":"2007","journal-title":"Proc Biol Sci"},{"issue":"1848","key":"ppat.1014290.ref043","first-page":"20162149","article-title":"Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival","volume":"284","author":"K Benaets","year":"2017","journal-title":"Proc Biol Sci"},{"key":"ppat.1014290.ref044","doi-asserted-by":"crossref","first-page":"766","DOI":"10.3389\/fmicb.2020.00766","article-title":"Interactions Between Thiamethoxam and Deformed Wing Virus Can Drastically Impair Flight Behavior of Honey Bees","volume":"11","author":"M Coulon","year":"2020","journal-title":"Front Microbiol"},{"issue":"32","key":"ppat.1014290.ref045","article-title":"Inapparent virus infections differentially affect honey bee flight","volume":"11","author":"NG Kaku","year":"2025","journal-title":"Sci Adv"},{"issue":"5","key":"ppat.1014290.ref046","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1111\/1758-2229.12434","article-title":"Flight performance of actively foraging honey bees is reduced by a common pathogen","volume":"8","author":"T Wells","year":"2016","journal-title":"Environ Microbiol Rep"},{"issue":"4","key":"ppat.1014290.ref047","doi-asserted-by":"crossref","first-page":"239","DOI":"10.3390\/insects11040239","article-title":"Diversity and Global Distribution of Viruses of the Western Honey Bee, Apis mellifera","volume":"11","author":"A Beaurepaire","year":"2020","journal-title":"Insects"},{"issue":"18","key":"ppat.1014290.ref048","doi-asserted-by":"crossref","first-page":"10241","DOI":"10.1002\/ece3.5544","article-title":"Seasonal dynamics and co-occurrence patterns of honey bee pathogens revealed by high-throughput RT-qPCR analysis","volume":"9","author":"P D\u2019Alvise","year":"2019","journal-title":"Ecol Evol"},{"issue":"10","key":"ppat.1014290.ref049","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0140272","article-title":"Four Categories of Viral Infection Describe the Health Status of Honey Bee Colonies","volume":"10","author":"E Amiri","year":"2015","journal-title":"PLoS One"},{"issue":"1","key":"ppat.1014290.ref050","doi-asserted-by":"crossref","first-page":"22","DOI":"10.4039\/tce.2015.23","article-title":"Occurrence, detection, and quantification of economically important viruses in healthy and unhealthy honey bee (Hymenoptera: Apidae) colonies in Canada","volume":"148","author":"SD Desai","year":"2015","journal-title":"Can Entomol"},{"key":"ppat.1014290.ref051","doi-asserted-by":"crossref","unstructured":"Dubois E, Dardouri M, Schurr F, Cougoule N, Sircoulomb F, Thi\u00e9ry R. Outcomes of honeybee pupae inoculated with deformed wing virus genotypes A and B. 2020.","DOI":"10.1007\/s13592-019-00701-z"},{"issue":"1895","key":"ppat.1014290.ref052","first-page":"20182452","article-title":"Direct transmission by injection affects competition among RNA viruses in honeybees","volume":"286","author":"EJ Remnant","year":"2019","journal-title":"Proc Biol Sci"},{"key":"ppat.1014290.ref053","doi-asserted-by":"crossref","DOI":"10.7717\/peerj.1591","article-title":"The Iflaviruses Sacbrood virus and Deformed wing virus evoke different transcriptional responses in the honeybee which may facilitate their horizontal or vertical transmission","volume":"4","author":"EV Ryabov","year":"2016","journal-title":"PeerJ"},{"issue":"12","key":"ppat.1014290.ref054","doi-asserted-by":"crossref","first-page":"7185","DOI":"10.1128\/AEM.70.12.7185-7191.2004","article-title":"Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France","volume":"70","author":"D Tentcheva","year":"2004","journal-title":"Appl Environ Microbiol"},{"key":"ppat.1014290.ref055","article-title":"Spatial distribution patterns of acute bee paralysis virus, black queen cell virus and sacbrood virus in Hesse, Germany","volume":"93","author":"R Siede","year":"2006","journal-title":"Vet Med Austria\/ Wien"},{"issue":"3","key":"ppat.1014290.ref056","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1051\/apido:2008007","article-title":"Incidence of acute bee paralysis virus, black queen cell virus, chronic bee paralysis virus, deformed wing virus, Kashmir bee virus and sacbrood virus in honey bees (Apis mellifera) in Denmark","volume":"39","author":"SL Nielsen","year":"2008","journal-title":"Apidologie"},{"issue":"6","key":"ppat.1014290.ref057","doi-asserted-by":"crossref","first-page":"330","DOI":"10.17221\/8248-VETMED","article-title":"A severe sacbrood virus outbreak in a honeybee (Apis mellifera L.) colony: A case report","volume":"60","author":"C Roy","year":"2015","journal-title":"Vet Med (Praha)"},{"issue":"1","key":"ppat.1014290.ref058","doi-asserted-by":"crossref","first-page":"231529","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":"V Doublet","year":"2024","journal-title":"R Soc Open Sci"},{"issue":"12","key":"ppat.1014290.ref059","doi-asserted-by":"crossref","first-page":"7185","DOI":"10.1128\/AEM.70.12.7185-7191.2004","article-title":"Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France","volume":"70","author":"D Tentcheva","year":"2004","journal-title":"Appl Environ Microbiol"},{"issue":"4","key":"ppat.1014290.ref060","doi-asserted-by":"crossref","first-page":"1881","DOI":"10.1021\/pr301226d","article-title":"An integrated proteomics reveals pathological mechanism of honeybee (Apis cerena) sacbrood disease","volume":"12","author":"B Han","year":"2013","journal-title":"J Proteome Res"},{"key":"ppat.1014290.ref061","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.jip.2017.09.006","article-title":"Chinese Sacbrood virus infection in Asian honey bees (Apis cerana cerana) and host immune responses to the virus infection","volume":"150","author":"L Shan","year":"2017","journal-title":"J Invertebr Pathol"},{"key":"ppat.1014290.ref062","doi-asserted-by":"crossref","first-page":"107687","DOI":"10.1016\/j.jip.2021.107687","article-title":"Sacbrood viruses cross-infection between Apis cerana and Apis mellifera: Rapid detection, viral dynamics, evolution and spillover risk assessment","volume":"186","author":"J-C Chang","year":"2021","journal-title":"J Invertebr Pathol"},{"key":"ppat.1014290.ref063","article-title":"Sacbrood Virus: A Growing Threat to Honeybees and Wild Pollinators","volume":"14","author":"R Wei","year":"2022","journal-title":"Viruses"},{"issue":"8","key":"ppat.1014290.ref064","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.3000003","article-title":"Why are RNA virus mutation rates so damn high?","volume":"16","author":"S Duffy","year":"2018","journal-title":"PLoS Biol"},{"issue":"1895","key":"ppat.1014290.ref065","first-page":"20182452","article-title":"Direct transmission by injection affects competition among RNA viruses in honeybees","volume":"286","author":"EJ Remnant","year":"2019","journal-title":"Proc Biol Sci"},{"key":"ppat.1014290.ref066","doi-asserted-by":"crossref","first-page":"104558","DOI":"10.1016\/j.meegid.2020.104558","article-title":"Egg transcriptome profile responds to maternal virus infection in honey bees, Apis mellifera","volume":"85","author":"E Amiri","year":"2020","journal-title":"Infect Genet Evol"},{"issue":"8","key":"ppat.1014290.ref067","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":"F Mondet","year":"2014","journal-title":"PLoS Pathog"},{"issue":"3","key":"ppat.1014290.ref068","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/s13592-016-0431-0","article-title":"Multiyear survey targeting disease incidence in US honey bees","volume":"47","author":"KS Traynor","year":"2016","journal-title":"Apidologie"},{"issue":"1","key":"ppat.1014290.ref069","doi-asserted-by":"crossref","first-page":"58","DOI":"10.2174\/1874285802115010058","article-title":"An Investigation of Honey Bee Viruses Prevalence in Managed Honey Bees (Apis mellifera and Apis cerana) Undergone Colony Decline","volume":"15","author":"C Yuan","year":"2021","journal-title":"TOMICROJ"},{"key":"ppat.1014290.ref070","doi-asserted-by":"crossref","DOI":"10.3390\/v15051217","article-title":"Viral co-infections and antiviral immunity in honey bees","volume":"15","author":"AM Durand","year":"2023","journal-title":"Viruses"},{"key":"ppat.1014290.ref071","first-page":"3416","article-title":"Parasitic and immune modulation of flight activity in honey bees tracked with optical counters","volume":"217","author":"C Alaux","year":"2014","journal-title":"J Exp Biol"},{"issue":"1","key":"ppat.1014290.ref072","doi-asserted-by":"crossref","first-page":"4804","DOI":"10.1038\/s41598-025-86937-5","article-title":"Genotype B of deformed wing virus and related recombinant viruses become dominant in European honey bee colonies","volume":"15","author":"F Sircoulomb","year":"2025","journal-title":"Sci Rep"},{"key":"ppat.1014290.ref073","article-title":"Deformed wing virus","author":"JR de Miranda","year":"2010","journal-title":"J Invertebr Pathol"},{"key":"ppat.1014290.ref074","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":"F Schurr","year":"2019","journal-title":"J Virol Methods"},{"issue":"3","key":"ppat.1014290.ref075","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1007\/s13592-012-0184-3","article-title":"Suitability of three common reference genes for quantitative real-time PCR in honey bees","volume":"44","author":"T Reim","year":"2012","journal-title":"Apidologie"},{"issue":"1","key":"ppat.1014290.ref076","doi-asserted-by":"crossref","first-page":"13935","DOI":"10.1038\/s41598-020-70965-4","article-title":"Reference gene selection for qRT-PCR analysis of season- and tissue-specific gene expression profiles in the honey bee Apis mellifera","volume":"10","author":"JH Jeon","year":"2020","journal-title":"Sci Rep"},{"issue":"24","key":"ppat.1014290.ref077","doi-asserted-by":"crossref","first-page":"4876","DOI":"10.1093\/nar\/25.24.4876","article-title":"The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools","volume":"25","author":"JD Thompson","year":"1997","journal-title":"Nucleic Acids Res"},{"issue":"4","key":"ppat.1014290.ref078","first-page":"357","article-title":"TreeView: an application to display phylogenetic trees on personal computers","volume":"12","author":"RD Page","year":"1996","journal-title":"Comput Appl Biosci"},{"key":"ppat.1014290.ref079","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1093\/jee\/18.2.265a","article-title":"A method of computing the effectiveness of an insecticide","volume":"18","author":"WS Abbott","year":"1925","journal-title":"J Econ Entomol"},{"issue":"3","key":"ppat.1014290.ref080","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1111\/j.1744-7348.1939.tb06990.x","article-title":"The Toxicity of Poisons Applied Jointly","volume":"26","author":"CI Bliss","year":"1939","journal-title":"Annals of Applied Biology"},{"issue":"1","key":"ppat.1014290.ref081","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1007\/s13592-019-00701-z","article-title":"Outcomes of honeybee pupae inoculated with deformed wing virus genotypes A and B","volume":"51","author":"E Dubois","year":"2019","journal-title":"Apidologie"},{"issue":"1","key":"ppat.1014290.ref082","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1111\/j.1744-7348.1972.tb01268.x","article-title":"Effects of sacbrood virus on adult honey\u2010bees","volume":"72","author":"L Bailey","year":"1972","journal-title":"Annals of Applied Biology"},{"issue":"3","key":"ppat.1014290.ref083","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1111\/j.1744-7348.1969.tb02844.x","article-title":"The multiplication and spread of sacbrood virus of bees","volume":"63","author":"L Bailey","year":"1969","journal-title":"Ann Appl Biol"},{"issue":"11","key":"ppat.1014290.ref084","doi-asserted-by":"crossref","first-page":"3427","DOI":"10.1073\/pnas.1422089112","article-title":"Rapid behavioral maturation accelerates failure of stressed honey bee colonies","volume":"112","author":"CJ Perry","year":"2015","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ppat.1014290.ref085","doi-asserted-by":"crossref","unstructured":"Locke B, Forsgren E, Miranda JRD. Increased tolerance and resistance to virus infections: a possible factor in the survival of Varroa destructor-resistant honey bees (Apis mellifera). 2014;9(6).","DOI":"10.1371\/journal.pone.0099998"},{"key":"ppat.1014290.ref086","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/1741-7007-6-50","article-title":"Modulation of social interactions by immune stimulation in honey bee, Apis mellifera, workers","volume":"6","author":"F-J Richard","year":"2008","journal-title":"BMC Biol"},{"issue":"1","key":"ppat.1014290.ref087","doi-asserted-by":"crossref","first-page":"8989","DOI":"10.1038\/s41598-021-88649-y","article-title":"Pupal cannibalism by worker honey bees contributes to the spread of deformed wing virus","volume":"11","author":"F Posada-Florez","year":"2021","journal-title":"Sci Rep"},{"issue":"1","key":"ppat.1014290.ref088","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1011061","article-title":"Promiscuous feeding on multiple adult honey bee hosts amplifies the vectorial capacity of Varroa destructor","volume":"19","author":"ZS Lamas","year":"2023","journal-title":"PLoS Pathog"},{"issue":"5494","key":"ppat.1014290.ref089","doi-asserted-by":"crossref","first-page":"1166","DOI":"10.1126\/science.290.5494.1166","article-title":"Survival for immunity: the price of immune system activation for bumblebee workers","volume":"290","author":"Y Moret","year":"2000","journal-title":"Science"},{"issue":"2","key":"ppat.1014290.ref090","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1007\/s13592-014-0318-x","article-title":"Immune responses of honeybees and their fitness costs as compared to bumblebees","volume":"46","author":"U Riessberger-Gall\u00e9","year":"2015","journal-title":"Apidologie"},{"issue":"12","key":"ppat.1014290.ref091","article-title":"A strong immune response in young adult honeybees masks their increased susceptibility to infection compared to older bees","volume":"8","author":"JC Bull","year":"2012","journal-title":"PLoS Pathog"},{"issue":"1","key":"ppat.1014290.ref092","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1186\/s12864-017-3597-6","article-title":"Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens","volume":"18","author":"V Doublet","year":"2017","journal-title":"BMC Genomics"},{"issue":"5","key":"ppat.1014290.ref093","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1016\/j.exger.2004.02.010","article-title":"Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees","volume":"39","author":"GV Amdam","year":"2004","journal-title":"Exp Gerontol"},{"issue":"12","key":"ppat.1014290.ref094","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1016\/j.exger.2005.08.004","article-title":"Social reversal of immunosenescence in honey bee workers","volume":"40","author":"GV Amdam","year":"2005","journal-title":"Exp Gerontol"},{"issue":"4","key":"ppat.1014290.ref095","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/S0022-5193(03)00121-8","article-title":"The hive bee to forager transition in honeybee colonies: the double repressor hypothesis","volume":"223","author":"GV Amdam","year":"2003","journal-title":"J Theor Biol"},{"key":"ppat.1014290.ref096","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.cois.2015.04.016","article-title":"Antiviral Defense Mechanisms in Honey Bees","volume":"10","author":"LM Brutscher","year":"2015","journal-title":"Curr Opin Insect Sci"},{"issue":"2","key":"ppat.1014290.ref097","doi-asserted-by":"crossref","first-page":"287","DOI":"10.3390\/v13020287","article-title":"Transcriptomic Responses of the Honey Bee Brain to Infection with Deformed Wing Virus","volume":"13","author":"MC Pizzorno","year":"2021","journal-title":"Viruses"},{"issue":"7","key":"ppat.1014290.ref098","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0288821","article-title":"Age-related response to mite parasitization and viral infection in the honey bee suggests a trade-off between growth and immunity","volume":"18","author":"V Zanni","year":"2023","journal-title":"PLoS One"},{"key":"ppat.1014290.ref099","doi-asserted-by":"crossref","first-page":"1149840","DOI":"10.3389\/fphys.2023.1149840","article-title":"Decoupling the effects of nutrition, age, and behavioral caste on honey bee physiology, immunity, and colony health","volume":"14","author":"M Corona","year":"2023","journal-title":"Front Physiol"}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1014290","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,6,25]],"date-time":"2026-06-25T17:23:11Z","timestamp":1782408191000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1014290"}},"subtitle":[],"editor":[{"given":"Ashley L.","family":"St. John","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,6,25]]},"references-count":99,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2026,6,25]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1014290","relation":{},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,6,25]]}}}