{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T20:57:05Z","timestamp":1782248225204,"version":"3.54.5"},"update-to":[{"DOI":"10.1371\/journal.ppat.1009973","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,4,25]],"date-time":"2022-04-25T00:00:00Z","timestamp":1650844800000}}],"reference-count":54,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2022,4,13]],"date-time":"2022-04-13T00:00:00Z","timestamp":1649808000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["HHSN272201400006C"],"award-info":[{"award-number":["HHSN272201400006C"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["75N93021C00018"],"award-info":[{"award-number":["75N93021C00018"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["HHSN272201400007C"],"award-info":[{"award-number":["HHSN272201400007C"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100012524","name":"American Lebanese Syrian Associated Charities","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100012524","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p>Wild birds can carry avian influenza viruses (AIV), including those with pandemic or panzootic potential, long distances. Even though AIV has a broad host range, few studies account for host diversity when estimating AIV spread. We analyzed AIV genomic sequences from North American wild birds, including 303 newly sequenced isolates, to estimate interspecies and geographic viral transition patterns among multiple co-circulating subtypes. Our results show high transition rates within Anseriformes and Charadriiformes, but limited transitions between these orders. Patterns of transition between species were positively associated with breeding habitat range overlap, and negatively associated with host genetic distance. Distance between regions (negative correlation) and summer temperature at origin (positive correlation) were strong predictors of transition between locations. Taken together, this study demonstrates that host diversity and ecology can determine evolutionary processes that underlie AIV natural history and spread. Understanding these processes can provide important insights for effective control of AIV.<\/jats:p>","DOI":"10.1371\/journal.ppat.1009973","type":"journal-article","created":{"date-parts":[[2022,4,13]],"date-time":"2022-04-13T13:53:56Z","timestamp":1649858036000},"page":"e1009973","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":26,"title":["Host diversity and behavior determine patterns of interspecies transmission and geographic diffusion of avian influenza A subtypes among North American wild reservoir species"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4815-8099","authenticated-orcid":true,"given":"Joseph T.","family":"Hicks","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kimberly","family":"Edwards","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6810-7304","authenticated-orcid":true,"given":"Xueting","family":"Qiu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7524-2379","authenticated-orcid":true,"given":"Do-Kyun","family":"Kim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James E.","family":"Hixson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott","family":"Krauss","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4397-7132","authenticated-orcid":true,"given":"Richard J.","family":"Webby","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1899-1856","authenticated-orcid":true,"given":"Robert G.","family":"Webster","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7572-4300","authenticated-orcid":true,"given":"Justin","family":"Bahl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,4,13]]},"reference":[{"issue":"1","key":"ppat.1009973.ref001","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1128\/mr.56.1.152-179.1992","article-title":"Evolution and ecology of influenza A viruses","volume":"56","author":"RG Webster","year":"1992","journal-title":"Microbiol Rev"},{"issue":"1416","key":"ppat.1009973.ref002","doi-asserted-by":"crossref","first-page":"1817","DOI":"10.1098\/rstb.2001.0997","article-title":"Emergence of influenza A viruses.","volume":"356","author":"RJ Webby","year":"2001","journal-title":"Philos Trans R Soc London Ser B Biol Sci"},{"key":"ppat.1009973.ref003","doi-asserted-by":"crossref","first-page":"84","DOI":"10.3389\/fvets.2018.00084","article-title":"Geographical and Historical Patterns in the Emergences of Novel Highly Pathogenic Avian Influenza (HPAI) H5 and H7 Viruses in Poultry.","volume":"5","author":"MS Dhingra","year":"2018","journal-title":"Front Vet Sci"},{"key":"ppat.1009973.ref004","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/j.meegid.2013.02.020","article-title":"Connecting the study of wild influenza with the potential for pandemic disease","volume":"17","author":"J Runstadler","year":"2013","journal-title":"Infect Genet Evol"},{"issue":"5","key":"ppat.1009973.ref005","doi-asserted-by":"crossref","first-page":"e1000076","DOI":"10.1371\/journal.ppat.1000076","article-title":"The Evolutionary Genetics and Emergence of Avian Influenza Viruses in Wild Birds.","volume":"4","author":"VG Dugan","year":"2008","journal-title":"PLoS Pathog"},{"issue":"6","key":"ppat.1009973.ref006","doi-asserted-by":"crossref","first-page":"533","DOI":"10.3109\/08830185.2010.507828","article-title":"Influenza Virus RNA Structure: Unique and Common Features.","volume":"29","author":"AP Gultyaev","year":"2010","journal-title":"Int Rev Immunol"},{"issue":"8","key":"ppat.1009973.ref007","doi-asserted-by":"crossref","first-page":"e1003570","DOI":"10.1371\/journal.ppat.1003570","article-title":"Influenza a virus migration and persistence in North American wild birds.","volume":"9","author":"J Bahl","year":"2013","journal-title":"PLoS Pathog"},{"issue":"1\u20132","key":"ppat.1009973.ref008","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.virusres.2005.05.013","article-title":"Phylogenetic analyses of type A influenza genes in natural reservoir species in North America reveals genetic variation","volume":"114","author":"E Spackman","year":"2005","journal-title":"Virus Res"},{"key":"ppat.1009973.ref009","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1186\/1471-2334-10-187","article-title":"Mapping the risk of avian influenza in wild birds in the US","volume":"10","author":"TL Fuller","year":"2010","journal-title":"BMC Infectious Diseases"},{"key":"ppat.1009973.ref010","doi-asserted-by":"crossref","first-page":"33161","DOI":"10.1038\/srep33161","article-title":"Application of Species Distribution Modeling for Avian Influenza surveillance in the United States considering the North America Migratory Flyways","volume":"6","author":"J Belkhiria","year":"2016","journal-title":"Scientific reports."},{"key":"ppat.1009973.ref011","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/1297-9716-44-42","article-title":"A global model of avian influenza prediction in wild birds: the importance of northern regions","volume":"44","author":"KA Herrick","year":"2013","journal-title":"Veterinary research"},{"key":"ppat.1009973.ref012","doi-asserted-by":"crossref","first-page":"e32729","DOI":"10.1371\/journal.pone.0032729","article-title":"Environmental and demographic determinants of avian influenza viruses in waterfowl across the contiguous united states","volume":"7","author":"ML Farnsworth","year":"2012","journal-title":"PLoS ONE."},{"issue":"1621","key":"ppat.1009973.ref013","doi-asserted-by":"crossref","first-page":"2003","DOI":"10.1098\/rspb.2007.0124","article-title":"Prevalence of avian influenza and host ecology","volume":"274","author":"LZ Garamszegi","year":"2007","journal-title":"Proc R Soc B Biol Sci"},{"issue":"7","key":"ppat.1009973.ref014","doi-asserted-by":"crossref","first-page":"1044","DOI":"10.1111\/1365-2656.12997","article-title":"Contrasting effects of host species and phylogenetic diversity on the occurrence of HPAI H5N1 in European wild birds","volume":"88","author":"ZYX Huang","year":"2019","journal-title":"J Anim Ecol"},{"issue":"1","key":"ppat.1009973.ref015","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1111\/j.1461-0248.2011.01703.x","article-title":"Migratory flyway and geographical distance are barriers to the gene flow of influenza virus among North American birds","volume":"15","author":"TT Lam","year":"2012","journal-title":"Ecol Lett"},{"issue":"2","key":"ppat.1009973.ref016","doi-asserted-by":"crossref","first-page":"e1003932","DOI":"10.1371\/journal.ppat.1003932","article-title":"Unifying viral genetics and human transportation data to predict the global transmission dynamics of human influenza H3N2.","volume":"10","author":"P Lemey","year":"2014","journal-title":"PLoS Pathog"},{"issue":"1","key":"ppat.1009973.ref017","first-page":"e65","article-title":"Emerging Concepts of Data Integration in Pathogen Phylodynamics","volume":"66","author":"G Baele","year":"2016","journal-title":"Syst Biol"},{"issue":"1","key":"ppat.1009973.ref018","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s12862-016-0845-3","article-title":"Quantifying predictors for the spatial diffusion of avian influenza virus in China","volume":"17","author":"L Lu","year":"2017","journal-title":"BMC Evol Biol"},{"issue":"2","key":"ppat.1009973.ref019","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1111\/tbed.12733","article-title":"Global genetic variation and transmission dynamics of H9N2 avian influenza virus.","volume":"65","author":"K Wei","year":"2018","journal-title":"Transbound Emerg Dis."},{"key":"ppat.1009973.ref020","doi-asserted-by":"crossref","first-page":"20120196","DOI":"10.1098\/rstb.2012.0196","article-title":"Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints","volume":"368","author":"NR Faria","year":"2013","journal-title":"Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences"},{"issue":"4","key":"ppat.1009973.ref021","doi-asserted-by":"crossref","first-page":"e1000346","DOI":"10.1371\/journal.pcbi.1000346","article-title":"The Role of Environmental Transmission in Recurrent Avian Influenza Epidemics.","volume":"5","author":"R Breban","year":"2009","journal-title":"PLoS Comput Biol"},{"issue":"8","key":"ppat.1009973.ref022","doi-asserted-by":"crossref","first-page":"e1001931","DOI":"10.1371\/journal.pbio.1001931","article-title":"Adaptive Evolution and Environmental Durability Jointly Structure Phylodynamic Patterns in Avian Influenza Viruses.","volume":"12","author":"B Roche","year":"2014","journal-title":"PLoS Biol"},{"issue":"2","key":"ppat.1009973.ref023","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/j.virol.2009.05.002","article-title":"Gene flow and competitive exclusion of avian influenza A virus in natural reservoir hosts","volume":"390","author":"J Bahl","year":"2009","journal-title":"Virology"},{"issue":"1","key":"ppat.1009973.ref024","doi-asserted-by":"crossref","DOI":"10.1186\/s12862-017-0965-4","article-title":"The impact of migratory flyways on the spread of avian influenza virus in North America","volume":"17","author":"M Fourment","year":"2017","journal-title":"BMC Evol Biol"},{"issue":"10","key":"ppat.1009973.ref025","first-page":"s7","article-title":"Population biology of emerging and re-emerging pathogens","volume":"10","author":"MEJ Woolhouse","year":"2002","journal-title":"Trends Microbiol"},{"key":"ppat.1009973.ref026","doi-asserted-by":"crossref","first-page":"e1004395","DOI":"10.1371\/journal.ppat.1004395","article-title":"The evolution and genetics of virus host shifts","author":"B Longdon","year":"2014","journal-title":"10, PLoS pathogens."},{"key":"ppat.1009973.ref027","doi-asserted-by":"crossref","first-page":"e1002260","DOI":"10.1371\/journal.ppat.1002260","article-title":"Host phylogeny determines viral persistence and replication in novel hosts","volume":"7","author":"B Longdon","year":"2011","journal-title":"PLoS Pathogens."},{"issue":"4","key":"ppat.1009973.ref028","first-page":"980","article-title":"A SIMPLE MODEL EXPLAINS THE DYNAMICS OF PREFERENTIAL HOST SWITCHING AMONG MAMMAL RNA VIRUSES","volume":"67","author":"JH Cuthill","year":"2013","journal-title":"Evolution (N Y)"},{"key":"ppat.1009973.ref029","doi-asserted-by":"crossref","first-page":"2910","DOI":"10.1128\/AEM.03790-13","article-title":"Abiotic factors affecting the persistence of avian influenza virus in surface waters of waterfowl habitats","volume":"80","author":"SP Keeler","year":"2014","journal-title":"Applied and Environmental Microbiology"},{"key":"ppat.1009973.ref030","doi-asserted-by":"crossref","first-page":"e0161929","DOI":"10.1371\/journal.pone.0161929","article-title":"Persistence of low pathogenic influenza A virus in water: a systematic review and quantitative meta-analysis","volume":"11","author":"AE Dalziel","year":"2016","journal-title":"PLoS One."},{"issue":"8","key":"ppat.1009973.ref031","doi-asserted-by":"crossref","first-page":"e104360","DOI":"10.1371\/journal.pone.0104360","article-title":"Large-Scale Avian Influenza Surveillance in Wild Birds throughout the United States","volume":"9","author":"SN Bevins","year":"2014","journal-title":"PLoS One"},{"issue":"5","key":"ppat.1009973.ref032","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"C. RE","year":"2004","journal-title":"Nucleic Acids Res"},{"issue":"9","key":"ppat.1009973.ref033","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1093\/bioinformatics\/btu033","article-title":"RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies","volume":"30","author":"A. Stamatakis","year":"2014","journal-title":"Bioinformatics"},{"issue":"1","key":"ppat.1009973.ref034","doi-asserted-by":"crossref","first-page":"vew007","DOI":"10.1093\/ve\/vew007","article-title":"Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen).","volume":"2","author":"A Rambaut","year":"2016","journal-title":"Virus Evol"},{"issue":"1","key":"ppat.1009973.ref035","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1111\/2041-210X.12299","article-title":"Split diversity in constrained conservation prioritization using integer linear programming.","volume":"6","author":"O Chernomor","year":"2015","journal-title":"Methods Ecol Evol"},{"key":"ppat.1009973.ref036","first-page":"1","article-title":"Permutational Multivariate Analysis of Variance (PERMANOVA)","author":"MJ Anderson","year":"2017","journal-title":"Wiley StatsRef: Statistics Reference Online"},{"issue":"6","key":"ppat.1009973.ref037","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/nmeth.4285","article-title":"ModelFinder: fast model selection for accurate phylogenetic estimates.","volume":"14","author":"S Kalyaanamoorthy","year":"2017","journal-title":"Nat Methods."},{"issue":"1","key":"ppat.1009973.ref038","doi-asserted-by":"crossref","first-page":"vey016","DOI":"10.1093\/ve\/vey016","article-title":"Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10.","volume":"4","author":"MA Suchard","year":"2018","journal-title":"Virus Evol"},{"key":"ppat.1009973.ref039","first-page":"57","volume-title":"Some Probabilistic and Statistical Problems in the Analysis of DNA Sequences.","author":"S. Tavar\u00e9","year":"1986"},{"issue":"1","key":"ppat.1009973.ref040","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1007\/BF02101990","article-title":"A new method for calculating evolutionary substitution rates","volume":"20","author":"C Lanave","year":"1984","journal-title":"J Mol Evol"},{"issue":"4","key":"ppat.1009973.ref041","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1016\/S0022-5193(05)80104-3","article-title":"The general stochastic model of nucleotide substitution","volume":"142","author":"F Rodr\u00edguez","year":"1990","journal-title":"J Theor Biol"},{"issue":"3988","key":"ppat.1009973.ref042","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1126\/science.172.3988.1089","article-title":"Fitting Discrete Probability Distributions to Evolutionary Events","volume":"172","author":"T Uzzell","year":"1971","journal-title":"Science (80-)"},{"issue":"1","key":"ppat.1009973.ref043","first-page":"82","article-title":"Limitations of the evolutionary parsimony method of phylogenetic analysis","volume":"7","author":"L Jin","year":"1990","journal-title":"Mol Biol Evol"},{"key":"ppat.1009973.ref044","doi-asserted-by":"crossref","first-page":"e88","DOI":"10.1371\/journal.pbio.0040088","article-title":"Relaxed phylogenetics and dating with confidence","volume":"4","author":"AJ Drummond","year":"2006","journal-title":"PLoS Biology"},{"issue":"A","key":"ppat.1009973.ref045","doi-asserted-by":"crossref","first-page":"27","DOI":"10.2307\/3213548","article-title":"On the Genealogy of Large Populations","volume":"19","author":"JFC Kingman","year":"1982","journal-title":"J Appl Probab"},{"issue":"3","key":"ppat.1009973.ref046","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1093\/genetics\/161.3.1307","article-title":"Estimating Mutation Parameters, Population History and Genealogy Simultaneously From Temporally Spaced Sequence Data","volume":"161","author":"AJ Drummond","year":"2002","journal-title":"Genetics"},{"issue":"1512","key":"ppat.1009973.ref047","doi-asserted-by":"crossref","first-page":"3985","DOI":"10.1098\/rstb.2008.0176","article-title":"Fast, accurate and simulation-free stochastic mapping.","volume":"363","author":"VN Minin","year":"2008","journal-title":"Philos Trans R Soc B Biol Sci"},{"issue":"3","key":"ppat.1009973.ref048","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1007\/s00285-007-0120-8","article-title":"Counting labeled transitions in continuous-time Markov models of evolution","volume":"56","author":"VN Minin","year":"2007","journal-title":"J Math Biol"},{"issue":"7424","key":"ppat.1009973.ref049","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1038\/nature11631","article-title":"The global diversity of birds in space and time","volume":"491","author":"W Jetz","year":"2012","journal-title":"Nature"},{"key":"ppat.1009973.ref050","unstructured":"BirdLife International and Handbook of the Birds of the World. Bird species distribution maps of the world. Version 6.0. [Internet]. Available from: http:\/\/datazone.birdlife.org\/species\/requestdis"},{"key":"ppat.1009973.ref051","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1175\/BAMS-87-3-343","article-title":"NORTH AMERICAN REGIONAL REANALYSIS","volume":"87","author":"F Mesinger","year":"2006","journal-title":"Bulletin of the American Meteorological Society"},{"key":"ppat.1009973.ref052","volume-title":"MOD13A3 MODIS\/Terra vegetation Indices Monthly L3 Global 1km SIN Grid V006","author":"K. Didan","year":"2015"},{"issue":"9","key":"ppat.1009973.ref053","doi-asserted-by":"crossref","first-page":"e1000520","DOI":"10.1371\/journal.pcbi.1000520","article-title":"Bayesian phylogeography finds its roots.","volume":"5","author":"P Lemey","year":"2009","journal-title":"PLoS Comput Biol"},{"key":"ppat.1009973.ref054","doi-asserted-by":"crossref","first-page":"e55","DOI":"10.7717\/peerj-cs.55","article-title":"Probabilistic programming in Python using PyMC3.","volume":"2","author":"J Salvatier","year":"2016","journal-title":"PeerJ Comput Sci"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1009973","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,4,25]],"date-time":"2022-04-25T00:00:00Z","timestamp":1650844800000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1009973","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,25]],"date-time":"2022-04-25T13:36:58Z","timestamp":1650893818000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1009973"}},"subtitle":[],"editor":[{"given":"Adi","family":"Stern","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,4,13]]},"references-count":54,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2022,4,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1009973","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.09.29.462321","asserted-by":"object"}]},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,13]]}}}