{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,1]],"date-time":"2026-07-01T12:24:16Z","timestamp":1782908656232,"version":"3.54.5"},"reference-count":51,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T00:00:00Z","timestamp":1759881600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>The Stockholm Paradigm, a multilevel framework for studying coevolutionary interactions, it is a promising method for obtaining a globally relevant understanding of the emergence of present and past host\u2013parasite and insect\u2013plant interactions. This research aimed to expand the application of the Paradigm to virus\u2013host interactions, considering that viruses are being subjected to the same evolutionary forces as any other living organism. By applying different data science techniques, we described and discussed capacity and opportunity traits for Influenza A H1N1 strains, and how they might influence the pathogen\u2019s host repertoire evolution, and thus ranked different strains according to their emergence risk in the human population. We hope to contribute to the application of different methods for understanding disease emergence, and consequently to the development of new public health strategies for preventing (re)emerging diseases.<\/jats:p>","DOI":"10.3390\/v17101350","type":"journal-article","created":{"date-parts":[[2025,10,8]],"date-time":"2025-10-08T12:04:52Z","timestamp":1759925092000},"page":"1350","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Stockholm Paradigm in the Study of Influenza H1N1 Viruses: A New Approach to the Study of Zoonotic Risk Coupling Multiple Correspondence Analysis and Multi-Locus Phylogenies"],"prefix":"10.3390","volume":"17","author":[{"given":"Sofia","family":"Galv\u00e3o Feronato","sequence":"first","affiliation":[{"name":"Grupo de Imunologia Molecular, Celular e Intelig\u00eancia Artificial, Instituto Carlos Chagas, Fiocruz\/PR, Curitiba 81350-010, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8307-1426","authenticated-orcid":false,"given":"Rafael Antunes","family":"Baggio","sequence":"additional","affiliation":[{"name":"CTPeixes, Instituto de Ci\u00eancias Biol\u00f3gicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6446-8660","authenticated-orcid":false,"given":"Hellen Geremias Gatica","family":"Santos","sequence":"additional","affiliation":[{"name":"Instituto Carlos Chagas, Funda\u00e7\u00e3o Oswaldo Cruz, Curitiba 81350-010, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1866-0563","authenticated-orcid":false,"given":"Guilherme","family":"Ferreira Silveira","sequence":"additional","affiliation":[{"name":"Grupo de Imunologia Molecular, Celular e Intelig\u00eancia Artificial, Instituto Carlos Chagas, Fiocruz\/PR, Curitiba 81350-010, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,10,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Feronato, S.G., and Silveira, G.F. (2023). From Darwinism to the Modern Age: How Evolutionary Paradigms Shape the Understanding of Host-Virus Coevolutionary Processes\u2013A Review. Preprints, 2023051188.","DOI":"10.20944\/preprints202305.1188.v2"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1727","DOI":"10.1111\/tbed.14146","article-title":"\u2018Accidents waiting to happen\u2019\u2014Insights from a simple model on the emergence of infectious agents in new hosts","volume":"69","author":"Feronato","year":"2022","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1890\/0012-9658(2000)081[0329:ROMDTV]2.0.CO;2","article-title":"Response of mallard ducklings to variation in habitat quality: An experiment of food limitation","volume":"81","author":"Elmberg","year":"2000","journal-title":"Ecology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.coisb.2018.11.001","article-title":"Climate change and emerging infectious diseases: Evolutionary complexity in action","volume":"13","author":"Brooks","year":"2019","journal-title":"Curr. Opin. Syst. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"308","DOI":"10.2307\/3565565","article-title":"On ecological fitting","volume":"45","author":"Janzen","year":"1985","journal-title":"Oikos"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1111\/j.2006.0030-1299.15025.x","article-title":"On ecological fitting, plant\u2013insect associations, herbivore host shifts, and host plant selection","volume":"114","author":"Agosta","year":"2006","journal-title":"Oikos"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"S76","DOI":"10.1890\/0012-9658(2006)87[76:EFAADO]2.0.CO;2","article-title":"Ecological fitting as a determinant of the community structure of platyhelminth parasites of anurans","volume":"87","author":"Brooks","year":"2006","journal-title":"Ecology"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Tilmon, K.J. (2008). Chapter 15. The Oscillation Hypothesis of Host-Plant Range and Speciation. Specialization, Speciation, and Radiation The Evolutionary Biology of Herbivorous Insects, University of California Press.","DOI":"10.1525\/9780520933828"},{"key":"ref_9","unstructured":"Ball, G.E. (1985). The taxon pulse: A general pattern of lineage radiation and extinction among carabid beetles. Taxonomy, Phylogeny, and Biogeography of Beetles and Ants: A Volume Dedicated to the Memory of Philip Jackson Darlington, Jr. 1904\u20131983, Dr. W. Junk Publishers."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1533","DOI":"10.1111\/j.1365-2699.2008.01951.x","article-title":"A macroevolutionary mosaic: Episodic host-switching, geographical colonization and diversification in complex host-parasite systems","volume":"35","author":"Hoberg","year":"2008","journal-title":"J. Biogeogr."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e1280","DOI":"10.1111\/tbed.14557","article-title":"Ecological super-spreaders drive host\u2013range oscillations: Omicron and risk space for emerging infectious disease","volume":"69","author":"Boeger","year":"2022","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Swayne, D.E. (2016). Influenza A virus. Animal Influenza, Wiley-Blackwell.","DOI":"10.1002\/9781118924341"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1038\/nrmicro.2017.118","article-title":"The evolution of seasonal influenza viruses","volume":"16","author":"Petrova","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_14","first-page":"991","article-title":"Diseases of humans and their domestic mammals: Pathogen characteristics, host range and the risk of emergence","volume":"356","author":"Cleaveland","year":"2001","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1111\/mam.12225","article-title":"Risk of human-to-wildlife transmission of SARS-CoV-2","volume":"51","author":"Gryseels","year":"2020","journal-title":"Mammal Rev."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Atkinson, P.W. (2010). The Global Threat of Emergent\/Re-emergent Vector-Borne Diseases. Vector Biology, Ecology and Control, Springer.","DOI":"10.1007\/978-90-481-2458-9"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Husson, F., L\u00ea, S., and Pag\u00e8s, J. (2017). Exploratory Multivariate Analysis by Example Using R, CRC Press.","DOI":"10.1201\/b21874"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"D466","DOI":"10.1093\/nar\/gkw857","article-title":"Influenza Research Database: An integrated bioinformatics resource for 107 influenza virus research","volume":"45","author":"Zhang","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"D678","DOI":"10.1093\/nar\/gkac1003","article-title":"Introducing the Bacterial and Viral Bioinformatics Resource Center (BV-BRC): A resource combining PATRIC, IRD and ViPR","volume":"51","author":"Olson","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_20","first-page":"1425","article-title":"Characterization, stability and convergence of hierarchical clustering methods","volume":"11","author":"Carlsson","year":"2010","journal-title":"J. Mach. Learn. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1002\/widm.53","article-title":"Algorithms for hierarchical clustering: An overview","volume":"2","author":"Murtagh","year":"2012","journal-title":"Wiley Interdiscip. Rev. Data Min. Knowl. Discov."},{"key":"ref_22","unstructured":"(2023, March 10). Geneious, Available online: https:\/\/www.geneious.com."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Bouckaert, R., Vaughan, T.G., Barido-Sottani, J., Duch\u00eane, S., Fourment, M., Gavryushkina, A., Heled, J., Jones, G., K\u00fchnert, D., and De Maio, N. (2019). BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol., 15.","DOI":"10.1371\/journal.pcbi.1006650"},{"key":"ref_25","unstructured":"Maddison, W.P., and Maddison, D.R. (2019). Mesquite: A Modular System for Evolutionary Analysis, Version 3.61, Mesquite Software, Inc.. Available online: http:\/\/www.mesquiteproject.org."},{"key":"ref_26","unstructured":"Brooks, D.R., Hoberg, E.P., and Boeger, W.A. (2019). The Stockholm Paradigm: Climate Change and Emerging Disease, University of Chicago Press. [1st ed.]. Available online: https:\/\/press.uchicago.edu\/ucp\/books\/book\/chicago\/S\/bo38871306.html."},{"key":"ref_27","first-page":"3","article-title":"The hemagglutinin: A determinant of pathogenicity","volume":"385","author":"Garten","year":"2014","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_28","first-page":"35","article-title":"Sialyloligossacharides of the respiratory epithelium in the selection of human influenza virus specificity","volume":"40","author":"Baum","year":"1990","journal-title":"Acta Histochem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/0168-1702(93)90056-S","article-title":"Influenza virus strains selectively recognize sialyologylossacharides on human respiratory epithelium: The role of the host cell in selection of hemagglutinin receptor specificity","volume":"29","author":"Couceiro","year":"1993","journal-title":"Virus Res."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Bullard, B.L., and Weaver, E.A. (2021). Strategies targeting hemagglutinin as a universal influenza vaccine. Vaccines, 9.","DOI":"10.3390\/vaccines9030257"},{"key":"ref_31","unstructured":"Abbas, A.L. (1991). Cellular and Molecular Immunology, HBJ International Edition."},{"key":"ref_32","first-page":"432","article-title":"Multiple Correspondence Analysis and its applications","volume":"10","author":"Kamalja","year":"2017","journal-title":"Electron. J. Appl. Stat. Anal."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1016\/j.jclepro.2018.10.357","article-title":"Measuring the circular economy-A Multiple Correspondence Analysis of 63 metrics","volume":"210","author":"Parchomenko","year":"2019","journal-title":"J. Clean. Prod."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1514","DOI":"10.1093\/aje\/kwu076","article-title":"Social Meets Molecular: Combining Phylogenetic and Latent Class Analyses to Understand HIV-1 Transmission in Switzerland","volume":"179","author":"Avila","year":"2014","journal-title":"Am. J. Epidemiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1093\/sysbio\/syaa019","article-title":"Bayesian Inference of Ancestral Host\u2013Parasite Interactions under a Phylogenetic Model of Host Repertoire Evolution","volume":"69","author":"Braga","year":"2020","journal-title":"Syst. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1007\/s11252-017-0683-0","article-title":"Agricultural food resources and the foraging ecologies of American black ducks (Anas rubripes) and mallards (Anas platyrhynchos) at the northern limits of their winter ranges","volume":"20","author":"English","year":"2017","journal-title":"Urban. Ecosyst."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1093\/auk\/122.3.949","article-title":"Phylogeography of the mallard (Anas platyrhynchos): Hybridization, dispersal, and lineage sorting contribute to complex geographic structure","volume":"122","author":"Kulikova","year":"2005","journal-title":"Auk"},{"key":"ref_38","unstructured":"Department for Environment and Water (2024, January 22). BDBSA SuperTables Overview, Available online: http:\/\/spatialwebapps.environment.sa.gov.au\/naturemaps\/?locale=en-us&viewer=naturemaps."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1002\/jwmg.21346","article-title":"Mallard survival, movements, and habitat use during autumn in Illinois","volume":"82","author":"Yetter","year":"2018","journal-title":"J. Wildl. Manag."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"411","DOI":"10.2307\/1369324","article-title":"Habitat use by mallards and American black ducks breeding in central Ontario","volume":"96","author":"Merendino","year":"1994","journal-title":"Condor"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Endo, A., and Nishiura, H. (2018). The role of migration in maintaining the transmission of avian influenza in waterfowl: A multisite multispecies transmission model along East Asian-Australian flyway. Can. J. Infect. Dis. Med. Microbiol., 2018.","DOI":"10.1155\/2018\/3420535"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1202","DOI":"10.2193\/0022-541X(2005)069[1202:ASASFO]2.0.CO;2","article-title":"Annual survival and site fidelity of northern pintails banded on the Yukon-Kuskokwim Delta, Alaska","volume":"69","author":"Nicolai","year":"2005","journal-title":"J. Wildl. Manag."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1002\/jwmg.752","article-title":"Exploring fall migratory patterns of American black ducks using eight decades of band-recovery data","volume":"78","author":"Lavretsky","year":"2014","journal-title":"J. Wildl. Manag."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1007\/s11252-006-0015-2","article-title":"Assessing the effect of developed habitat on waterbird behaviour in an urban riparian system in Ottawa, Canada","volume":"10","author":"Donaldson","year":"2007","journal-title":"Urban. Econ."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/j.ecoenv.2016.10.038","article-title":"Mallards (Anas platyrhynchos) and wastewater ponds, Part I: Mallard ducks overwintering at a northern wastewater treatment pond","volume":"143","author":"Welsh","year":"2017","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_46","first-page":"79","article-title":"American black duck Anas rubripes and mallard A. platyrhynchos abundance, occurrence of heterospecific pairing and wetland use between 1976 and 2003 in northeastern Nova Scotia, Canada","volume":"56","author":"Seymour","year":"2006","journal-title":"Wildfowl"},{"key":"ref_47","first-page":"152","article-title":"Interspecific territoriality and competitive interactions between American black ducks Anas rubripes and mallard A. platyrhynchos","volume":"43","author":"Seymour","year":"1992","journal-title":"Wildfowl"},{"key":"ref_48","first-page":"87","article-title":"Feral Mallards: A risk for hybridisation with wild Pacific Black Ducks in Australia?","volume":"126","author":"Guay","year":"2009","journal-title":"Victorian Nat."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Ramasamy, R. (2014). Zoonotic malaria\u2014Global overview and research and policy needs. Front. Public Health, 2.","DOI":"10.3389\/fpubh.2014.00123"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.antiviral.2016.03.010","article-title":"Zika Virus: History, Emergence, Biology, and Prospects for Control","volume":"130","author":"Weaver","year":"2016","journal-title":"Antivir. Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"17","DOI":"10.15252\/emmm.201404792","article-title":"Investigating the zoonotic origin of the West African Ebola epidemic","volume":"7","author":"Weiss","year":"2015","journal-title":"EMBO Mol. Med."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/17\/10\/1350\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:50:25Z","timestamp":1760035825000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/17\/10\/1350"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,8]]},"references-count":51,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,10]]}},"alternative-id":["v17101350"],"URL":"https:\/\/doi.org\/10.3390\/v17101350","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,8]]}}}