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Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2020,5,12]]},"abstract":"<jats:p>Anthropogenic changes create evolutionarily novel environments that present opportunities for emerging diseases, potentially changing the balance between host and pathogen. Honey bees provide essential pollination services, but intensification and globalization of honey bee management has coincided with increased pathogen pressure, primarily due to a parasitic mite\/virus complex. Here, we investigated how honey bee individual and group phenotypes are altered by a virus of concern, Israeli acute paralysis virus (IAPV). Using automated and manual behavioral monitoring of IAPV-inoculated individuals, we find evidence for pathogen manipulation of worker behavior by IAPV, and reveal that this effect depends on social context; that is, within versus between colony interactions. Experimental inoculation reduced social contacts between honey bee colony members, suggesting an adaptive host social immune response to diminish transmission. Parallel analyses with double-stranded RNA (dsRNA)-immunostimulated bees revealed these behaviors are part of a generalized social immune defensive response. Conversely, inoculated bees presented to groups of bees from other colonies experienced reduced aggression compared with dsRNA-immunostimulated bees, facilitating entry into susceptible colonies. This reduction was associated with a shift in cuticular hydrocarbons, the chemical signatures used by bees to discriminate colony members from intruders. These responses were specific to IAPV infection, suggestive of pathogen manipulation of the host. Emerging bee pathogens may thus shape host phenotypes to increase transmission, a strategy especially well-suited to the unnaturally high colony densities of modern apiculture. These findings demonstrate how anthropogenic changes could affect arms races between human-managed hosts and their pathogens to potentially affect global food security.<\/jats:p>","DOI":"10.1073\/pnas.2002268117","type":"journal-article","created":{"date-parts":[[2020,4,27]],"date-time":"2020-04-27T20:25:34Z","timestamp":1588019134000},"page":"10406-10413","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":109,"title":["Honey bee virus causes context-dependent changes in host social behavior"],"prefix":"10.1073","volume":"117","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8734-8058","authenticated-orcid":false,"given":"Amy C.","family":"Geffre","sequence":"first","affiliation":[{"name":"Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50011;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5977-3900","authenticated-orcid":false,"given":"Tim","family":"Gernat","sequence":"additional","affiliation":[{"name":"Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana\u2013Champaign, Urbana, IL 61801;"},{"name":"Faculty of Mathematics and Computer Science, Department of Computer Science, University of Leipzig, 04109 Leipzig, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0811-7372","authenticated-orcid":false,"given":"Gyan P.","family":"Harwood","sequence":"additional","affiliation":[{"name":"Department of Entomology, University of Illinois at Urbana\u2013Champaign, Urbana, IL 61801;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2925-0807","authenticated-orcid":false,"given":"Beryl M.","family":"Jones","sequence":"additional","affiliation":[{"name":"Program in Ecology, Evolution, and Conservation Biology, University of Illinois, Urbana\u2013Champaign, IL 61801;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5771-8182","authenticated-orcid":false,"given":"Deisy","family":"Morselli Gysi","sequence":"additional","affiliation":[{"name":"Faculty of Mathematics and Computer Science, Department of Computer Science, University of Leipzig, 04109 Leipzig, Germany;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam R.","family":"Hamilton","sequence":"additional","affiliation":[{"name":"Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana\u2013Champaign, Urbana, IL 61801;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9956-9613","authenticated-orcid":false,"given":"Bryony C.","family":"Bonning","sequence":"additional","affiliation":[{"name":"Department of Entomology and Nematology, University of Florida, Gainesville, FL 32611;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amy L.","family":"Toth","sequence":"additional","affiliation":[{"name":"Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50011;"},{"name":"Department of Entomology, Iowa State University, Ames, IA 50011;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4828-4068","authenticated-orcid":false,"given":"Gene E.","family":"Robinson","sequence":"additional","affiliation":[{"name":"Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana\u2013Champaign, Urbana, IL 61801;"},{"name":"Department of Entomology, University of Illinois at Urbana\u2013Champaign, Urbana, IL 61801;"},{"name":"Neuroscience Program, University of Illinois at Urbana\u2013Champaign, Urbana, IL 61801"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6164-1344","authenticated-orcid":false,"given":"Adam G.","family":"Dolezal","sequence":"additional","affiliation":[{"name":"Department of Entomology, University of Illinois at Urbana\u2013Champaign, Urbana, IL 61801;"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2020,4,27]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/S0001-706X(00)00179-0","article-title":"Anthropogenic environmental change and the emergence of infectious diseases in wildlife","volume":"78","author":"Daszak P.","year":"2001","unstructured":"P. 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Rep."},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1093\/ajae\/aas031","article-title":"Honey bee pollination markets and the internalization of reciprocal benefits","volume":"94","author":"Rucker R. R.","year":"2012","unstructured":"R. R. Rucker, W. N. Thurman, M. Burgett, Honey bee pollination markets and the internalization of reciprocal benefits. Am. J. Agric. Econ. 94, 956\u2013977 (2012).","journal-title":"Am. J. Agric. Econ."},{"key":"e_1_3_4_11_2","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 C. M.","year":"2019","unstructured":"C. M. Grozinger, M. L. Flenniken, Bee viruses: Ecology, pathogenicity, and impacts. Annu. Rev. Entomol. 64, 205\u2013226 (2019).","journal-title":"Annu. Rev. 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Graham, Are dispersal mechanisms changing the host-parasite relationship and increasing the virulence of Varroa destructor (Mesostigmata: Varroidae) in managed honey bee (Hymenoptera: Apidae) colonies? Environ. Entomol. 46, 737\u2013746 (2017).","journal-title":"Environ. Entomol."},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1146\/annurev.mi.41.100187.002205","article-title":"Rapid evolution of RNA viruses","volume":"41","author":"Steinhauer D. A.","year":"1987","unstructured":"D. A. Steinhauer, J. J. Holland, Rapid evolution of RNA viruses. Annu. Rev. Microbiol. 41, 409\u2013433 (1987).","journal-title":"Annu. Rev. Microbiol."},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"e1004261","DOI":"10.1371\/journal.ppat.1004261","article-title":"Israeli acute paralysis virus: Epidemiology, pathogenesis and implications for honey bee health","volume":"10","author":"Chen Y. P.","year":"2014","unstructured":"Y. P. 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Pathol. 103 (suppl. 1), S120\u2013S131 (2010).","journal-title":"J. Invertebr. Pathol."},{"key":"e_1_3_4_22_2","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 J. R.","year":"2010","unstructured":"J. R. de Miranda, E. Genersch, Deformed wing virus. J. Invertebr. Pathol. 103 (suppl. 1), S48\u2013S61 (2010).","journal-title":"J. Invertebr. Pathol."},{"key":"e_1_3_4_23_2","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1007\/s000400050076","article-title":"Drifting of honeybees","volume":"45","author":"Pfeiffer K. J.","year":"1998","unstructured":"K. J. Pfeiffer, K. Crailsheim, Drifting of honeybees. Insectes Soc. 45, 151\u2013167 (1998).","journal-title":"Insectes Soc."},{"key":"e_1_3_4_24_2","first-page":"1517","article-title":"Virus infection causes specific learning deficits in honeybee foragers","volume":"274","author":"Iqbal J.","year":"2007","unstructured":"J. Iqbal, U. Mueller, Virus infection causes specific learning deficits in honeybee foragers. Proc. Biol. Sci. 274, 1517\u20131521 (2007).","journal-title":"Proc. Biol. Sci."},{"key":"e_1_3_4_25_2","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1007\/s00359-006-0192-8","article-title":"The parasitic mite Varroa destructor affects non-associative learning in honey bee foragers, Apis mellifera L","volume":"193","author":"Kralj J.","year":"2007","unstructured":"J. Kralj, A. Brockmann, S. Fuchs, J. Tautz, The parasitic mite Varroa destructor affects non-associative learning in honey bee foragers, Apis mellifera L. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 193, 363\u2013370 (2007).","journal-title":"J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol."},{"key":"e_1_3_4_26_2","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":"Perry C. J.","year":"2015","unstructured":"C. J. Perry, E. S\u00f8vik, M. R. Myerscough, A. B. Barron, Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc. Natl. Acad. Sci. U.S.A. 112, 3427\u20133432 (2015).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_4_27_2","doi-asserted-by":"crossref","first-page":"1538","DOI":"10.1111\/j.1420-9101.2010.02022.x","article-title":"Altruistic self-removal of health-compromised honey bee workers from their hive","volume":"23","author":"Rueppell O.","year":"2010","unstructured":"O. Rueppell, M. K. Hayworth, N. P. Ross, Altruistic self-removal of health-compromised honey bee workers from their hive. J. Evol. Biol. 23, 1538\u20131546 (2010).","journal-title":"J. Evol. Biol."},{"key":"e_1_3_4_28_2","first-page":"20162149","article-title":"Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival","volume":"284","author":"Benaets K.","year":"2017","unstructured":"K. Benaets ., Covert deformed wing virus infections have long-term deleterious effects on honeybee foraging and survival. Proc. Biol. Sci. 284 20162149 (2017).","journal-title":"Proc. Biol. Sci."},{"key":"e_1_3_4_29_2","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1007\/s13592-016-0475-1","article-title":"Should I stay or should I go: Honeybee drifting behaviour as a function of parasitism","volume":"48","author":"Bordier C.","year":"2017","unstructured":"C. Bordier, M. Pioz, D. Crauser, Y. Le Conte, C. Alaux, Should I stay or should I go: Honeybee drifting behaviour as a function of parasitism. Apidologie 48, 286\u2013297 (2017).","journal-title":"Apidologie"},{"key":"e_1_3_4_30_2","first-page":"xxi","volume-title":"The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies","author":"H\u00f6lldobler B.","year":"2009","unstructured":"B. H\u00f6lldobler, E. O. Wilson, The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies (W.W. Norton, New York, ed. 1, 2009), pp. xxi.","edition":"1"},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/978-3-319-17599-7_9","volume-title":"Social Recognition in Invertebrates: The Knowns and the Unknowns","author":"Breed M. D.","year":"2015","unstructured":"M. D. Breed, C. N. Cook, H. F. McCreery, M. Rodriguez, \u201cNestmate recognition in eusocial insects: The honeybee as a model system\u201d in Social Recognition in Invertebrates: The Knowns and the Unknowns, L. Aquiloni, E. Tricarico, Eds. (Springer International Publishing, Cham, 2015), pp. 147\u2013164."},{"key":"e_1_3_4_32_2","doi-asserted-by":"crossref","first-page":"e41855","DOI":"10.7554\/eLife.41855","article-title":"The cuticular hydrocarbon profiles of honey bee workers develop via a socially-modulated innate process","volume":"8","author":"Vernier C. L.","year":"2019","unstructured":"C. L. Vernier ., The cuticular hydrocarbon profiles of honey bee workers develop via a socially-modulated innate process. eLife 8, e41855 (2019).","journal-title":"eLife"},{"key":"e_1_3_4_33_2","unstructured":"A. Dolezal . Honey bee virus causes context-dependent changes in host social behavior. Dryad. https:\/\/doi.org\/10.5061\/dryad.m63xsj3z8. Deposited 6 March 2020."},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1126\/science.aat4793","article-title":"Social network plasticity decreases disease transmission in a eusocial insect","volume":"362","author":"Stroeymeyt N.","year":"2018","unstructured":"N. Stroeymeyt ., Social network plasticity decreases disease transmission in a eusocial insect. Science 362, 941\u2013945 (2018).","journal-title":"Science"},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.jip.2006.03.010","article-title":"Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera","volume":"92","author":"Chen Y.","year":"2006","unstructured":"Y. Chen, J. Evans, M. Feldlaufer, Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J. Invertebr. Pathol. 92, 152\u2013159 (2006).","journal-title":"J. Invertebr. Pathol."},{"key":"e_1_3_4_36_2","doi-asserted-by":"crossref","first-page":"9","DOI":"10.3390\/insects10010009","article-title":"Israeli acute paralysis virus: Honey bee queen\u2212worker interaction and potential virus transmission pathways","volume":"10","author":"Amiri E.","year":"2019","unstructured":"E. Amiri ., Israeli acute paralysis virus: Honey bee queen\u2212worker interaction and potential virus transmission pathways. Insects 10, 9 (2019).","journal-title":"Insects"},{"key":"e_1_3_4_37_2","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.jip.2013.07.006","article-title":"Arthropod viruses and small RNAs","volume":"114","author":"Vijayendran D.","year":"2013","unstructured":"D. Vijayendran, P. M. Airs, K. Dolezal, B. C. Bonning, Arthropod viruses and small RNAs. J. Invertebr. Pathol. 114, 186\u2013195 (2013).","journal-title":"J. Invertebr. 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Science 336, 1304\u20131306 (2012).","journal-title":"Science"},{"key":"e_1_3_4_53_2","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1126\/science.246.4926.109","article-title":"Hormonal and genetic control of behavioral integration in honey bee colonies","volume":"246","author":"Robinson G. E.","year":"1989","unstructured":"G. E. Robinson, R. E. Page, Jr, C. Strambi, A. Strambi, Hormonal and genetic control of behavioral integration in honey bee colonies. Science 246, 109\u2013112 (1989).","journal-title":"Science"},{"key":"e_1_3_4_54_2","doi-asserted-by":"crossref","first-page":"22265","DOI":"10.1038\/srep22265","article-title":"In vivo and in vitro infection dynamics of honey bee viruses","volume":"6","author":"Carrillo-Tripp J.","year":"2016","unstructured":"J. Carrillo-Tripp ., In vivo and in vitro infection dynamics of honey bee viruses. Sci. Rep. 6, 22265 (2016).","journal-title":"Sci. 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Ecol."},{"key":"e_1_3_4_61_2","doi-asserted-by":"crossref","first-page":"1589","DOI":"10.1016\/j.jinsphys.2012.09.014","article-title":"Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies","volume":"58","author":"Baracchi D.","year":"2012","unstructured":"D. Baracchi, A. Fadda, S. Turillazzi, Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies. J. Insect Physiol. 58, 1589\u20131596 (2012).","journal-title":"J. Insect Physiol."},{"key":"e_1_3_4_62_2","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1186\/1472-6785-13-25","article-title":"Ecto- and endoparasite induce similar chemical and brain neurogenomic responses in the honey bee (Apis mellifera)","volume":"13","author":"McDonnell C. M.","year":"2013","unstructured":"C. M. McDonnell ., Ecto- and endoparasite induce similar chemical and brain neurogenomic responses in the honey bee (Apis mellifera). 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