{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,31]],"date-time":"2025-12-31T11:18:29Z","timestamp":1767179909666,"version":"build-2238731810"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1006876","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2019,3,28]],"date-time":"2019-03-28T00:00:00Z","timestamp":1553731200000}}],"reference-count":59,"publisher":"Public Library of Science (PLoS)","issue":"3","license":[{"start":{"date-parts":[[2019,3,18]],"date-time":"2019-03-18T00:00:00Z","timestamp":1552867200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000913","name":"James S. McDonnell Foundation","doi-asserted-by":"crossref","award":["220020325"],"award-info":[{"award-number":["220020325"]}],"id":[{"id":"10.13039\/100000913","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100010198","name":"Ministerio de Econom\u00eda, Industria y Competitividad, Gobierno de Espa\u00f1a","doi-asserted-by":"crossref","award":["FIS2014-57686-P"],"award-info":[{"award-number":["FIS2014-57686-P"]}],"id":[{"id":"10.13039\/501100010198","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100010198","name":"Ministerio de Econom\u00eda, Industria y Competitividad, Gobierno de Espa\u00f1a","doi-asserted-by":"crossref","award":["FIS2015-71582-C2-1"],"award-info":[{"award-number":["FIS2015-71582-C2-1"]}],"id":[{"id":"10.13039\/501100010198","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100006531","name":"Departament d\u2019Universitats, Recerca i Societat de la Informaci\u00f3","doi-asserted-by":"publisher","award":["2017-SGR-896"],"award-info":[{"award-number":["2017-SGR-896"]}],"id":[{"id":"10.13039\/501100006531","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007512","name":"Universitat Rovira i Virgili","doi-asserted-by":"crossref","award":["2017PFR-URV-B2-41"],"award-info":[{"award-number":["2017PFR-URV-B2-41"]}],"id":[{"id":"10.13039\/501100007512","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100003030","name":"Ag\u00e8ncia de Gesti\u00f3 d\u2019Ajuts Universitaris i de Recerca","doi-asserted-by":"publisher","award":["ICREA Academia"],"award-info":[{"award-number":["ICREA Academia"]}],"id":[{"id":"10.13039\/501100003030","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"DOI":"10.1371\/journal.pcbi.1006876","type":"journal-article","created":{"date-parts":[[2019,3,18]],"date-time":"2019-03-18T13:57:12Z","timestamp":1552917432000},"page":"e1006876","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["Endemicity and prevalence of multipartite viruses under heterogeneous between-host transmission"],"prefix":"10.1371","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9246-6195","authenticated-orcid":true,"given":"Eugenio","family":"Valdano","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Susanna","family":"Manrubia","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1820-0062","authenticated-orcid":true,"given":"Sergio","family":"G\u00f3mez","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0937-0334","authenticated-orcid":true,"given":"Alex","family":"Arenas","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2019,3,18]]},"reference":[{"issue":"2","key":"ref1","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/0042-6822(66)90161-9","article-title":"Possible relationships of virus-specific products of tobacco rattle virus infections","volume":"28","author":"R Lister","year":"1966","journal-title":"Virology"},{"issue":"11","key":"ref2","doi-asserted-by":"crossref","first-page":"e1005819","DOI":"10.1371\/journal.ppat.1005819","article-title":"The strange lifestyle of multipartite viruses","volume":"12","author":"A Sicard","year":"2016","journal-title":"PLoS Pathog"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"228","DOI":"10.3390\/v8080228","article-title":"Ins and outs of multipartite positive-strand RNA plant viruses: packaging versus systemic spread","volume":"8","author":"M Dall\u2019Ara","year":"2016","journal-title":"Viruses"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"5004","DOI":"10.1038\/s41598-017-05335-8","article-title":"Within-host evolution of segments ratio for the tripartite genome of alfalfa mosaic virus","volume":"7","author":"B Wu","year":"2017","journal-title":"Sci Rep"},{"issue":"1","key":"ref5","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1038\/s41540-017-0035-y","article-title":"Multipartite viruses: adaptive trick or evolutionary treat?","volume":"3","author":"A Luc\u00eda-Sanz","year":"2017","journal-title":"NPJ Syst Biol Appl"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.coviro.2018.07.018","article-title":"Theoretical approaches to disclosing the emergence and adaptive advantages of multipartite viruses","volume":"33","author":"A Luc\u00eda-Sanz","year":"2018","journal-title":"Curr Opin Virol"},{"key":"ref7","article-title":"Plant virology","author":"R Hull","year":"2013"},{"issue":"2","key":"ref8","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1111\/j.1364-3703.2007.00455.x","article-title":"Citrus tristeza virus: a pathogen that changed the course of the citrus industry","volume":"9","author":"P Moreno","year":"2008","journal-title":"Mol Plant Pathol"},{"issue":"8","key":"ref9","doi-asserted-by":"crossref","first-page":"e1000125","DOI":"10.1371\/journal.ppat.1000125","article-title":"Diversification of rice yellow mottle virus and related viruses spans the history of agriculture from the neolithic to the present","volume":"4","author":"D Fargette","year":"2008","journal-title":"PLoS Pathog"},{"issue":"12","key":"ref10","doi-asserted-by":"crossref","first-page":"6177","DOI":"10.1128\/JVI.02160-09","article-title":"Long-term evolution of the Luteoviridae: time scale and mode of virus speciation","volume":"84","author":"I Pag\u00e1n","year":"2010","journal-title":"J Virol"},{"issue":"6","key":"ref11","doi-asserted-by":"crossref","first-page":"e2523","DOI":"10.1371\/journal.pone.0002523","article-title":"The prehistory of potyviruses: their initial radiation was during the dawn of agriculture","volume":"3","author":"AJ Gibbs","year":"2008","journal-title":"PLOS ONE"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1146\/annurev.phyto.43.040204.140238","article-title":"The current and future dynamics of disease in plant communities","volume":"44","author":"JJ Burdon","year":"2006","journal-title":"Annu Rev Phytopathol"},{"issue":"2","key":"ref13","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.virusres.2008.07.028","article-title":"Plant virus emergence and evolution: origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control","volume":"141","author":"RA Jones","year":"2009","journal-title":"Virus Res"},{"issue":"7","key":"ref14","doi-asserted-by":"crossref","first-page":"e1002796","DOI":"10.1371\/journal.ppat.1002796","article-title":"Effect of biodiversity changes in disease risk: exploring disease emergence in a plant-virus system","volume":"8","author":"I Pag\u00e1n","year":"2012","journal-title":"PLoS Pathog"},{"issue":"3","key":"ref15","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1007\/s10658-013-0317-1","article-title":"Plant-virus interactions and the agro-ecological interface","volume":"138","author":"H Alexander","year":"2014","journal-title":"Eur J Plant Pathol"},{"issue":"1","key":"ref16","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1038\/ismej.2017.155","article-title":"Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale","volume":"12","author":"P Bernardo","year":"2017","journal-title":"ISME J"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1146\/annurev.mi.27.100173.000533","article-title":"Defective interfering viruses","volume":"27","author":"AS Huang","year":"1973","journal-title":"Annu Rev Microbiol"},{"key":"ref18","first-page":"151","article-title":"Origin and replication of defective interfering particles","volume":"93","author":"J Perrault","year":"1981","journal-title":"Curr Top Microbiol Immunol"},{"key":"ref19","first-page":"175","article-title":"RNA Genetics: Volume II: Retroviruses, Viroids, and RNA Recombination","author":"S Schlesinger","year":"2018"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"11678","DOI":"10.1128\/JVI.78.21.11678-11685.2004","article-title":"Evolutionary transition toward defective RNAs that are infectious by complementation","volume":"78","author":"J Garc\u00eda-Arriaza","year":"2004","journal-title":"J Virol"},{"issue":"1743","key":"ref21","doi-asserted-by":"crossref","first-page":"3812","DOI":"10.1098\/rspb.2012.1086","article-title":"Evolutionary dynamics of genome segmentation in multipartite viruses","volume":"279","author":"J Iranzo","year":"2012","journal-title":"Proc R Soc Lond B Biol Sci"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/S0022-5193(05)80424-2","article-title":"Levels of selection, evolution of sex in RNA viruses and the origin of life","volume":"153","author":"L Chao","year":"1991","journal-title":"J Theor Biol"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1007\/BF02257374","article-title":"Divided genomes and intrinsic noise","volume":"20","author":"J Pressing","year":"1984","journal-title":"J Mol Evol"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"S5","DOI":"10.1017\/S0031182000072978","article-title":"The evolutionary biology of molecular parasites","volume":"100","author":"S Nee","year":"1990","journal-title":"Parasitol"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"e1001344","DOI":"10.1371\/journal.pgen.1001344","article-title":"Viral genome segmentation can result from a trade-off between genetic content and particle stability","volume":"7","author":"S Ojosnegros","year":"2011","journal-title":"PLoS Genet"},{"issue":"19","key":"ref26","doi-asserted-by":"crossref","first-page":"9719","DOI":"10.1128\/JVI.00780-15","article-title":"Circulative nonpropagative aphid transmission of nanoviruses: an oversimplified view","volume":"89","author":"A Sicard","year":"2015","journal-title":"J Virol"},{"issue":"45","key":"ref27","doi-asserted-by":"crossref","first-page":"17891","DOI":"10.1073\/pnas.0702739104","article-title":"Estimation of the number of virus particles transmitted by an insect vector","volume":"104","author":"B Moury","year":"2007","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1548","key":"ref28","doi-asserted-by":"crossref","first-page":"1943","DOI":"10.1098\/rstb.2010.0076","article-title":"Pathways to extinction: beyond the error threshold","volume":"365","author":"SC Manrubia","year":"2010","journal-title":"Philos Trans R Soc Lond, B, Biol Sci"},{"issue":"16","key":"ref29","doi-asserted-by":"crossref","first-page":"e00561","DOI":"10.1128\/JVI.00561-17","article-title":"The number of target molecules of the amplification step limits accuracy and sensitivity in ultra deep sequencing viral population studies","volume":"91","author":"R Gallet","year":"2017","journal-title":"Journal of virology"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"146","DOI":"10.3390\/f8050146","article-title":"Spatial heterogeneity of the forest canopy scales with the heterogeneity of an understory shrub based on fractal analysis","volume":"8","author":"CK Denny","year":"2017","journal-title":"Forests"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"GB1009","DOI":"10.1029\/2003GB002108","article-title":"Geographic distribution of major crops across the world","volume":"18","author":"B Leff","year":"2004","journal-title":"Global Biogeochem Cycles"},{"issue":"6","key":"ref32","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1046\/j.1365-3059.2001.00613.x","article-title":"Synergism between plant viruses: a mathematical analysis of the epidemiological implications","volume":"50","author":"XS Zhang","year":"2001","journal-title":"Plant Pathology"},{"issue":"6934","key":"ref33","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1038\/nature01542","article-title":"Ecological interference between fatal diseases","volume":"422","author":"P Rohani","year":"2003","journal-title":"Nature"},{"issue":"10","key":"ref34","first-page":"1","article-title":"Threshold effects for two pathogens spreading on a network","volume":"95","author":"MEJ Newman","year":"2005","journal-title":"Phys Rev Lett"},{"issue":"5805","key":"ref35","doi-asserted-by":"crossref","first-page":"1603","DOI":"10.1126\/science.1132338","article-title":"Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa","volume":"314","author":"LJ Abu-Raddad","year":"2006","journal-title":"Science"},{"issue":"3","key":"ref36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1103\/PhysRevE.84.036106","article-title":"Competing epidemics on complex networks","volume":"84","author":"B Karrer","year":"2011","journal-title":"Phys Rev E"},{"issue":"8","key":"ref37","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pcbi.1003169","article-title":"Host mobility drives pathogen competition in spatially structured populations","volume":"9","author":"C Poletto","year":"2013","journal-title":"PLoS Comput Biol"},{"issue":"1781","key":"ref38","doi-asserted-by":"crossref","first-page":"20133374","DOI":"10.1098\/rspb.2013.3374","article-title":"Frequency-dependent assistance as a way out of competitive exclusion between two strains of an emerging virus","volume":"281","author":"F P\u00e9r\u00e9farres","year":"2014","journal-title":"Proceedings of the Royal Society of London B: Biological Sciences"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1016\/j.jtbi.2017.02.011","article-title":"Exposing the diversity of multiple infection patterns","volume":"419","author":"MT Sofonea","year":"2017","journal-title":"J Theor Biol"},{"issue":"5","key":"ref40","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1016\/j.tim.2017.02.003","article-title":"Collective infectious units in viruses","volume":"25","author":"R Sanju\u00e1n","year":"2017","journal-title":"Trends Microbiol"},{"issue":"14","key":"ref41","doi-asserted-by":"crossref","first-page":"3200","DOI":"10.1103\/PhysRevLett.86.3200","article-title":"Epidemic spreading in scale-free networks","volume":"86","author":"R Pastor-Satorras","year":"2001","journal-title":"Phys Rev Lett"},{"issue":"1","key":"ref42","doi-asserted-by":"crossref","first-page":"16128","DOI":"10.1103\/PhysRevE.66.016128","article-title":"Spread of epidemic disease on networks","volume":"66","author":"MEJ Newman","year":"2002","journal-title":"Phys Rev E"},{"issue":"3","key":"ref43","doi-asserted-by":"crossref","first-page":"925","DOI":"10.1103\/RevModPhys.87.925","article-title":"Epidemic processes in complex networks","volume":"87","author":"R Pastor-Satorras","year":"2015","journal-title":"Rev Mod Phys"},{"key":"ref44","doi-asserted-by":"crossref","DOI":"10.1017\/CBO9780511791383","article-title":"Dynamical processes on complex networks","author":"A Barrat","year":"2008"},{"issue":"12","key":"ref45","doi-asserted-by":"crossref","first-page":"4448","DOI":"10.1073\/pnas.0408871102","article-title":"Suppression of viral infectivity through lethal defection","volume":"102","author":"A Grande-P\u00e9rez","year":"2005","journal-title":"Proc Natl Acad Sci USA"},{"issue":"1","key":"ref46","doi-asserted-by":"crossref","first-page":"18001","DOI":"10.1209\/0295-5075\/85\/18001","article-title":"Stochastic extinction of viral infectivity through the action of defectors","volume":"85","author":"J Iranzo","year":"2008","journal-title":"Europhys Lett"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1038\/nrg3605","article-title":"Evolution of crop species: genetics of domestication and diversification","volume":"14","author":"RS Meyer","year":"2013","journal-title":"Nat Rev Genet"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1128\/JVI.43.1.18-25.1982","article-title":"Isolation and characterization of defective simian virus 40 genomes which complement for infectivity","volume":"43","author":"FJ O\u2019Neill","year":"1982","journal-title":"J Virol"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"3253","DOI":"10.1073\/pnas.88.8.3253","article-title":"Complementation between Sindbis viral RNAs produces infectious particles with a bipartite genome","volume":"88","author":"U Geigenm\u00fcller-Gnirke","year":"1991","journal-title":"Proc Nat Acad Sci USA"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"3922","DOI":"10.1128\/JVI.71.5.3922-3931.1997","article-title":"Assembled coronavirus from complementation of two defective interfering RNAs","volume":"71","author":"KH Kim","year":"1997","journal-title":"J Virol"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1099\/00221287-27-3-477","article-title":"Properties and behaviour of a virus depending for its multiplication on another","volume":"27","author":"B Kassanis","year":"1962","journal-title":"J Gen Microbiol"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"1825","DOI":"10.1016\/j.febslet.2009.05.045","article-title":"Evolution of geminiviruses and their satellites","volume":"583","author":"MS Nawaz-ul Rehman","year":"2009","journal-title":"FEBS Lett"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1038\/nature07218","article-title":"The virophage as a unique parasite of the giant mimivirus","volume":"455","author":"BL Scola","year":"2008","journal-title":"Nature"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"200","DOI":"10.4161\/rna.8.2.14238","article-title":"Rolling-circle replication of viroids, viroid-like satellite RNAs and hepatitis delta virus: Variations on a theme","volume":"8","author":"R Flores","year":"2011","journal-title":"RNA Biol"},{"key":"ref55","first-page":"314","article-title":"Plant virus biodiversity and ecology","volume":"4","author":"JD Wren","year":"2006","journal-title":"PLoS Biol"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1111\/j.1420-9101.2008.01658.x","article-title":"Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future","volume":"22","author":"S Alizon","year":"2009","journal-title":"J Evol Biol"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"066117","DOI":"10.1103\/PhysRevE.63.066117","article-title":"Epidemic dynamics and endemic states in complex networks","volume":"63","author":"R Pastor-Satorras","year":"2001","journal-title":"Phys Rev E"},{"issue":"1","key":"ref58","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1090\/S0002-9947-1942-0006633-7","article-title":"Topics in the theory of Markoff chains","volume":"52","author":"JL Doob","year":"1942","journal-title":"Trans Am Math Soc"},{"issue":"10","key":"ref59","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pcbi.1004579","article-title":"Temporal Gillespie algorithm: fast simulation of contagion processes on time-varying networks","volume":"11","author":"CL Vestergaard","year":"2015","journal-title":"PLoS Comput Biol"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1006876","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2019,3,28]],"date-time":"2019-03-28T00:00:00Z","timestamp":1553731200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pcbi.1006876","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,12,1]],"date-time":"2020-12-01T15:37:27Z","timestamp":1606837047000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1006876"}},"subtitle":[],"editor":[{"given":"Rob J.","family":"De Boer","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2019,3,18]]},"references-count":59,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2019,3,18]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1006876","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,3,18]]}}}