Integrating influenza antigenic dynamics with molecular evolution

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Abstract

Trevor Bedford1,*,†author-9070, Marc A Suchard2,3,4author-4087, Philippe Lemey5author-4914, Gytis Dudas1author-4915, Victoria Gregory6author-4916, Alan J Hay6author-4917, John W McCauley6author-4918, Colin A Russell7,8author-4919, Derek J Smith7,9,10author-4920 and Andrew Rambaut1,11,12author-47691Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom2Department of Biomathematics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States3Department of Human Genetics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States4Department of Biostatistics, UCLA Fielding School of Public Health, University of California, Los Angeles, Los Angeles, United States5Department of Microbiology and Immunology, Rega Institute, Katholieke Universiteit Leuven, Leuven, Belgium6Division of Virology, MRC National Institute for Medical Research, London, United Kingdom7WHO Collaborating Centre for Modeling, Evolution and Control of Emerging Infectious Diseases, University of Cambridge, Cambridge, United Kingdom8Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom9Centre for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge, United Kingdom10Department of Virology, Erasmus Medical Centre, Rotterdam, Netherlands11Fogarty International Center, National Institutes of Health, Bethesda, United States12Centre for Immunity, Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom↵*For correspondence: tbedford{at}fhcrc.orgRichard Losick, Reviewing editorHarvard University, United States↵TB, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents↵DJS, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents↵AR, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents↵MAS, Conception and design, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents↵PL, Conception and design, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents↵GD, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article↵VG, Acquisition of data, Contributed unpublished essential data or reagents↵AJH, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents↵JWMC, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents↵CAR, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article, Contributed unpublished essential data or reagents↵† Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, United StatesAbstractInfluenza viruses undergo continual antigenic evolution allowing mutant viruses to evade host immunity acquired to previous virus strains. Antigenic phenotype is often assessed through pairwise measurement of cross-reactivity between influenza strains using the hemagglutination inhibition (HI) assay. Here, we extend previous approaches to antigenic cartography, and simultaneously characterize antigenic and genetic evolution by modeling the diffusion of antigenic phenotype over a shared virus phylogeny. Using HI data from influenza lineages A/H3N2, A/H1N1, B/Victoria and B/Yamagata, we determine patterns of antigenic drift across viral lineages, showing that A/H3N2 evolves faster and in a more punctuated fashion than other influenza lineages. We also show that year-to-year antigenic drift appears to drive incidence patterns within each influe za lineage. This work makes possible substantial future advances in investigating the dynamics of influenza and other antigenically-variable pathogens by providing a model that intimately combines molecular and antigenic evolution.DOI: http://dx.doi.org/10.7554/eLife.01914.001Author keywordsinfluenzaevolutionantigenic cartographyphylogeneticsBayesian inferencemultidimensional scalingResearch organismvirusesFootnotes↵The authors declare that no competing interests exist.Received November 19, 2013.Accepted December 18, 2013.Copyright © 2013, Bedford et alThis article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.