Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus

Martha I. Nelson, Lone Simonsen, Cecile Viboud, Mark Miller, Jill Taylor, Kirsten St. George, Sara B. Griesemer, Elodie Ghedin, Naomi A. Sengamalay, David J. Spiro, Igor Volkov, Bryan T. Grenfell, David J. Lipman, Jeffery K. Taubenberger, Edward C. Holmes

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

Resumé

Understanding the evolutionary dynamics of influenza A virus is central to its surveillance and control. While immune-driven antigenic drift is a key determinant of viral evolution across epidemic seasons, the evolutionary processes shaping influenza virus diversity within seasons are less clear. Here we show with a phylogenetic analysis of 413 complete genomes of human H3N2 influenza A viruses collected between 1997 and 2005 from New York State, United States, that genetic diversity is both abundant and largely generated through the seasonal importation of multiple divergent clades of the same subtype. These clades cocirculated within New York State, allowing frequent reassortment and generating genome-wide diversity. However, relatively low levels of positive selection and genetic diversity were observed at amino acid sites considered important in antigenic drift. These results indicate that adaptive evolution occurs only sporadically in influenza A virus; rather, the stochastic processes of viral migration and clade reassortment play a vital role in shaping short-term evolutionary dynamics. Thus, predicting future patterns of influenza virus evolution for vaccine strain selection is inherently complex and requires intensive surveillance, whole-genome sequencing, and phenotypic analysis.
OriginalsprogEngelsk
TidsskriftPLOS Pathogens
Vol/bind2
Udgave nummer12
Antal sider8
ISSN1553-7366
DOI
StatusUdgivet - 2006
Udgivet eksterntJa

Citer dette

Nelson, Martha I. ; Simonsen, Lone ; Viboud, Cecile ; Miller, Mark ; Taylor, Jill ; St. George, Kirsten ; Griesemer, Sara B. ; Ghedin, Elodie ; Sengamalay, Naomi A. ; Spiro, David J. ; Volkov, Igor ; Grenfell, Bryan T. ; Lipman, David J. ; Taubenberger, Jeffery K. ; Holmes, Edward C. / Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus. I: PLOS Pathogens. 2006 ; Bind 2, Nr. 12.
@article{ecec751dda834bc396eabc7c702a84eb,
title = "Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus",
abstract = "Understanding the evolutionary dynamics of influenza A virus is central to its surveillance and control. While immune-driven antigenic drift is a key determinant of viral evolution across epidemic seasons, the evolutionary processes shaping influenza virus diversity within seasons are less clear. Here we show with a phylogenetic analysis of 413 complete genomes of human H3N2 influenza A viruses collected between 1997 and 2005 from New York State, United States, that genetic diversity is both abundant and largely generated through the seasonal importation of multiple divergent clades of the same subtype. These clades cocirculated within New York State, allowing frequent reassortment and generating genome-wide diversity. However, relatively low levels of positive selection and genetic diversity were observed at amino acid sites considered important in antigenic drift. These results indicate that adaptive evolution occurs only sporadically in influenza A virus; rather, the stochastic processes of viral migration and clade reassortment play a vital role in shaping short-term evolutionary dynamics. Thus, predicting future patterns of influenza virus evolution for vaccine strain selection is inherently complex and requires intensive surveillance, whole-genome sequencing, and phenotypic analysis.",
author = "Nelson, {Martha I.} and Lone Simonsen and Cecile Viboud and Mark Miller and Jill Taylor and {St. George}, Kirsten and Griesemer, {Sara B.} and Elodie Ghedin and Sengamalay, {Naomi A.} and Spiro, {David J.} and Igor Volkov and Grenfell, {Bryan T.} and Lipman, {David J.} and Taubenberger, {Jeffery K.} and Holmes, {Edward C.}",
year = "2006",
doi = "10.1371/journal.ppat.0020125",
language = "English",
volume = "2",
journal = "PLOS Pathogens",
issn = "1553-7366",
publisher = "Public Library of Science",
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Nelson, MI, Simonsen, L, Viboud, C, Miller, M, Taylor, J, St. George, K, Griesemer, SB, Ghedin, E, Sengamalay, NA, Spiro, DJ, Volkov, I, Grenfell, BT, Lipman, DJ, Taubenberger, JK & Holmes, EC 2006, 'Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus', PLOS Pathogens, bind 2, nr. 12. https://doi.org/10.1371/journal.ppat.0020125

Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus. / Nelson, Martha I.; Simonsen, Lone; Viboud, Cecile; Miller, Mark; Taylor, Jill; St. George, Kirsten; Griesemer, Sara B.; Ghedin, Elodie; Sengamalay, Naomi A.; Spiro, David J.; Volkov, Igor; Grenfell, Bryan T.; Lipman, David J.; Taubenberger, Jeffery K.; Holmes, Edward C.

I: PLOS Pathogens, Bind 2, Nr. 12, 2006.

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus

AU - Nelson, Martha I.

AU - Simonsen, Lone

AU - Viboud, Cecile

AU - Miller, Mark

AU - Taylor, Jill

AU - St. George, Kirsten

AU - Griesemer, Sara B.

AU - Ghedin, Elodie

AU - Sengamalay, Naomi A.

AU - Spiro, David J.

AU - Volkov, Igor

AU - Grenfell, Bryan T.

AU - Lipman, David J.

AU - Taubenberger, Jeffery K.

AU - Holmes, Edward C.

PY - 2006

Y1 - 2006

N2 - Understanding the evolutionary dynamics of influenza A virus is central to its surveillance and control. While immune-driven antigenic drift is a key determinant of viral evolution across epidemic seasons, the evolutionary processes shaping influenza virus diversity within seasons are less clear. Here we show with a phylogenetic analysis of 413 complete genomes of human H3N2 influenza A viruses collected between 1997 and 2005 from New York State, United States, that genetic diversity is both abundant and largely generated through the seasonal importation of multiple divergent clades of the same subtype. These clades cocirculated within New York State, allowing frequent reassortment and generating genome-wide diversity. However, relatively low levels of positive selection and genetic diversity were observed at amino acid sites considered important in antigenic drift. These results indicate that adaptive evolution occurs only sporadically in influenza A virus; rather, the stochastic processes of viral migration and clade reassortment play a vital role in shaping short-term evolutionary dynamics. Thus, predicting future patterns of influenza virus evolution for vaccine strain selection is inherently complex and requires intensive surveillance, whole-genome sequencing, and phenotypic analysis.

AB - Understanding the evolutionary dynamics of influenza A virus is central to its surveillance and control. While immune-driven antigenic drift is a key determinant of viral evolution across epidemic seasons, the evolutionary processes shaping influenza virus diversity within seasons are less clear. Here we show with a phylogenetic analysis of 413 complete genomes of human H3N2 influenza A viruses collected between 1997 and 2005 from New York State, United States, that genetic diversity is both abundant and largely generated through the seasonal importation of multiple divergent clades of the same subtype. These clades cocirculated within New York State, allowing frequent reassortment and generating genome-wide diversity. However, relatively low levels of positive selection and genetic diversity were observed at amino acid sites considered important in antigenic drift. These results indicate that adaptive evolution occurs only sporadically in influenza A virus; rather, the stochastic processes of viral migration and clade reassortment play a vital role in shaping short-term evolutionary dynamics. Thus, predicting future patterns of influenza virus evolution for vaccine strain selection is inherently complex and requires intensive surveillance, whole-genome sequencing, and phenotypic analysis.

U2 - 10.1371/journal.ppat.0020125

DO - 10.1371/journal.ppat.0020125

M3 - Journal article

VL - 2

JO - PLOS Pathogens

JF - PLOS Pathogens

SN - 1553-7366

IS - 12

ER -