The Evolutionary Dynamics of Human Influenza B Virus
Despite their close phylogenetic relationship, type A and B influenza viruses exhibit major epidemiological differences in humans, with the latter both less common and less often associated with severe disease. However, it is unclear what processes determine the evolutionary dynamics of influenza B virus, and how influenza viruses A and B interact at the evolutionary scale. To address these questions we inferred the phylogenetic history of human influenza B virus using complete genome sequences for which the date (day) of isolation was available. By comparing the phylogenetic patterns of all eight viral segments we determined the occurrence of segment reassortment over a 30-year sampling period. An analysis of rates of nucleotide substitution and selection pressures revealed sporadic occurrences of adaptive evolution, most notably in the viral hemagglutinin and compatible with the action of antigenic drift, yet lower rates of overall and nonsynonymous nucleotide substitution compared to influenza A virus. Overall, these results led us to propose a model in which evolutionary changes within and between the antigenically distinct ‘Yam88’ and ‘Vic87’ lineages of influenza B virus are the result of changes in herd immunity, with reassortment continuously generating novel genetic variation. Additionally, we suggest that the interaction with influenza A virus may be central in shaping the evolutionary dynamics of influenza B virus, facilitating the shift of dominance between the Vic87 and the Yam88 lineages.
KeywordsInfluenza B virus Phylogeny Reassortment Coalescent Antigenic drift Epidemiology
We thank Dr. J. K. Taubenberger for constructive comments on an earlier version of the manuscript and Dr. C. Viboud for assistance with the epidemiological data. We thank all those involved in the Influenza Genome Sequencing Project for contributing their viruses or obtaining genome sequence data. This work was supported in part by NIH Grant GM080533-01.
- Ghedin E, Sengamalay N, Shumway M, Zaborsky J, Feldblyum T, Subbu V, Spiro D, Sitz J, Koo H, Bolotov P, Dernovoy D, Tatusova T, Bao Y, St George K, Taylor J, Lipman D, Fraser C, Taubenberger J, Salzberg S (2005) Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 437:1162–1166PubMedCrossRefGoogle Scholar
- Holmes EC, Ghedin E, Miller N, Taylor J, Bao Y, St George K, Grenfell BT, Salzberg SL, Fraser CM, Lipman DJ, Taubenberger JK (2005) Whole-genome analysis of human influenza A virus reveals multiple persistent lineage and reassortment among recent H3N2 viruses. PLoS Biol 3:e300PubMedCrossRefGoogle Scholar
- Lindstrom SE, Hiromoto Y, Nishimura H, Saito T, Nerome R, Nerome K (1999) Comparative analysis of evolutionary mechanisms of the hemagglutinin and three internal protein genes of influenza B virus: multiple cocirculating lineages and frequent reassortment of the NP, M, and NS genes. J Virol 73:4413–4426PubMedGoogle Scholar
- Maddison DR, Maddison WP (2001) MacClade 4: analysis of phylogeny and character evolution. Version 4.03. Sinauer Associates, Sunderland, MAGoogle Scholar
- McCullers JA, Wang GC, He S, Webster RG (1999) Reassortment and insertion-deletion are strategies for the evolution of influenza B viruses in nature. J Virol 73:7374–7348Google Scholar
- Nelson MI, Simonsen L, Viboud C, Miller MA, Taylor J, St. George K, Griesemer EG, Ghedin E, Sengamalay NA et al (2006) Stochastic processes are key determinants of short-term evolution in Influenza A virus. PLoS Pathog 2:e125Google Scholar
- Rambaut A (1996) Se–Al: Sequence Alignment Editor. Available at: http://www.evolve.zoo.ox.ac.uk/
- Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, MAGoogle Scholar