Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans

Justin Bahl, Martha I. Nelson, Kwok H. Chan, Rubing Chen, Dhanasekaran Vijaykrishna, Rebecca A. Halpin, Timothy B. Stockwell, Xudong Lin, David E. Wentworth, Elodie Ghedin, Yi Guan, J. S Malik Peiris, Steven Riley, Andrew Rambaut, Edward C. Holmes, Gavin J D Smith

Research output: Contribution to journalArticle

Abstract

Populations of seasonal influenza virus experience strong annual bottlenecks that pose a considerable extinction risk. It has been suggested that an influenza source population located in tropical Southeast or East Asia seeds annual temperate epidemics. Here we investigate the seasonal dynamics and migration patterns of influenza A H3N2 virus by analysis of virus samples obtained from 2003 to 2006 from Australia, Europe, Japan, New York, New Zealand, Southeast Asia, and newly sequenced viruses from Hong Kong. In contrast to annual temperate epidemics, relatively low levels of relative genetic diversity and no seasonal fluctuations characterized virus populations in tropical Southeast Asia and Hong Kong. Bayesian phylogeographic analysis using discrete temporal and spatial characters reveal high rates of viral migration between urban centers tested. Although the virus population that migrated between Southeast Asia and Hong Kong persisted through time, this was dependent on virus input from temperate regions and these tropical regions did not maintain a source for annual H3N2 influenza epidemics. We further show that multiple lineages may seed annual influenza epidemics, and that each region may function as a potential source population. We therefore propose that the global persistence of H3N2 influenza A virus is the result of a migrating metapopulation in which multiple different localities may seed seasonal epidemics in temperate regions in a given year. Such complex global migration dynamics may confound control efforts and contribute to the emergence and spread of antigenic variants and drug-resistant viruses.

Original languageEnglish (US)
Pages (from-to)19359-19364
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number48
DOIs
StatePublished - Nov 29 2011

Fingerprint

H3N2 Subtype Influenza A Virus
Influenza A virus
Southeastern Asia
Viruses
Hong Kong
Human Influenza
Seeds
Population
Bayes Theorem
Far East
Orthomyxoviridae
New Zealand
Japan
Pharmaceutical Preparations

Keywords

  • Evolution
  • Molecular epidemiology
  • Phylogeography
  • Source-sink

ASJC Scopus subject areas

  • General

Cite this

Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans. / Bahl, Justin; Nelson, Martha I.; Chan, Kwok H.; Chen, Rubing; Vijaykrishna, Dhanasekaran; Halpin, Rebecca A.; Stockwell, Timothy B.; Lin, Xudong; Wentworth, David E.; Ghedin, Elodie; Guan, Yi; Peiris, J. S Malik; Riley, Steven; Rambaut, Andrew; Holmes, Edward C.; Smith, Gavin J D.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 48, 29.11.2011, p. 19359-19364.

Research output: Contribution to journalArticle

Bahl, J, Nelson, MI, Chan, KH, Chen, R, Vijaykrishna, D, Halpin, RA, Stockwell, TB, Lin, X, Wentworth, DE, Ghedin, E, Guan, Y, Peiris, JSM, Riley, S, Rambaut, A, Holmes, EC & Smith, GJD 2011, 'Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans', Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 48, pp. 19359-19364. https://doi.org/10.1073/pnas.1109314108
Bahl, Justin ; Nelson, Martha I. ; Chan, Kwok H. ; Chen, Rubing ; Vijaykrishna, Dhanasekaran ; Halpin, Rebecca A. ; Stockwell, Timothy B. ; Lin, Xudong ; Wentworth, David E. ; Ghedin, Elodie ; Guan, Yi ; Peiris, J. S Malik ; Riley, Steven ; Rambaut, Andrew ; Holmes, Edward C. ; Smith, Gavin J D. / Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans. In: Proceedings of the National Academy of Sciences of the United States of America. 2011 ; Vol. 108, No. 48. pp. 19359-19364.
@article{b94bb158ef444dfca67d65a10b3594ba,
title = "Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans",
abstract = "Populations of seasonal influenza virus experience strong annual bottlenecks that pose a considerable extinction risk. It has been suggested that an influenza source population located in tropical Southeast or East Asia seeds annual temperate epidemics. Here we investigate the seasonal dynamics and migration patterns of influenza A H3N2 virus by analysis of virus samples obtained from 2003 to 2006 from Australia, Europe, Japan, New York, New Zealand, Southeast Asia, and newly sequenced viruses from Hong Kong. In contrast to annual temperate epidemics, relatively low levels of relative genetic diversity and no seasonal fluctuations characterized virus populations in tropical Southeast Asia and Hong Kong. Bayesian phylogeographic analysis using discrete temporal and spatial characters reveal high rates of viral migration between urban centers tested. Although the virus population that migrated between Southeast Asia and Hong Kong persisted through time, this was dependent on virus input from temperate regions and these tropical regions did not maintain a source for annual H3N2 influenza epidemics. We further show that multiple lineages may seed annual influenza epidemics, and that each region may function as a potential source population. We therefore propose that the global persistence of H3N2 influenza A virus is the result of a migrating metapopulation in which multiple different localities may seed seasonal epidemics in temperate regions in a given year. Such complex global migration dynamics may confound control efforts and contribute to the emergence and spread of antigenic variants and drug-resistant viruses.",
keywords = "Evolution, Molecular epidemiology, Phylogeography, Source-sink",
author = "Justin Bahl and Nelson, {Martha I.} and Chan, {Kwok H.} and Rubing Chen and Dhanasekaran Vijaykrishna and Halpin, {Rebecca A.} and Stockwell, {Timothy B.} and Xudong Lin and Wentworth, {David E.} and Elodie Ghedin and Yi Guan and Peiris, {J. S Malik} and Steven Riley and Andrew Rambaut and Holmes, {Edward C.} and Smith, {Gavin J D}",
year = "2011",
month = "11",
day = "29",
doi = "10.1073/pnas.1109314108",
language = "English (US)",
volume = "108",
pages = "19359--19364",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "48",

}

TY - JOUR

T1 - Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans

AU - Bahl, Justin

AU - Nelson, Martha I.

AU - Chan, Kwok H.

AU - Chen, Rubing

AU - Vijaykrishna, Dhanasekaran

AU - Halpin, Rebecca A.

AU - Stockwell, Timothy B.

AU - Lin, Xudong

AU - Wentworth, David E.

AU - Ghedin, Elodie

AU - Guan, Yi

AU - Peiris, J. S Malik

AU - Riley, Steven

AU - Rambaut, Andrew

AU - Holmes, Edward C.

AU - Smith, Gavin J D

PY - 2011/11/29

Y1 - 2011/11/29

N2 - Populations of seasonal influenza virus experience strong annual bottlenecks that pose a considerable extinction risk. It has been suggested that an influenza source population located in tropical Southeast or East Asia seeds annual temperate epidemics. Here we investigate the seasonal dynamics and migration patterns of influenza A H3N2 virus by analysis of virus samples obtained from 2003 to 2006 from Australia, Europe, Japan, New York, New Zealand, Southeast Asia, and newly sequenced viruses from Hong Kong. In contrast to annual temperate epidemics, relatively low levels of relative genetic diversity and no seasonal fluctuations characterized virus populations in tropical Southeast Asia and Hong Kong. Bayesian phylogeographic analysis using discrete temporal and spatial characters reveal high rates of viral migration between urban centers tested. Although the virus population that migrated between Southeast Asia and Hong Kong persisted through time, this was dependent on virus input from temperate regions and these tropical regions did not maintain a source for annual H3N2 influenza epidemics. We further show that multiple lineages may seed annual influenza epidemics, and that each region may function as a potential source population. We therefore propose that the global persistence of H3N2 influenza A virus is the result of a migrating metapopulation in which multiple different localities may seed seasonal epidemics in temperate regions in a given year. Such complex global migration dynamics may confound control efforts and contribute to the emergence and spread of antigenic variants and drug-resistant viruses.

AB - Populations of seasonal influenza virus experience strong annual bottlenecks that pose a considerable extinction risk. It has been suggested that an influenza source population located in tropical Southeast or East Asia seeds annual temperate epidemics. Here we investigate the seasonal dynamics and migration patterns of influenza A H3N2 virus by analysis of virus samples obtained from 2003 to 2006 from Australia, Europe, Japan, New York, New Zealand, Southeast Asia, and newly sequenced viruses from Hong Kong. In contrast to annual temperate epidemics, relatively low levels of relative genetic diversity and no seasonal fluctuations characterized virus populations in tropical Southeast Asia and Hong Kong. Bayesian phylogeographic analysis using discrete temporal and spatial characters reveal high rates of viral migration between urban centers tested. Although the virus population that migrated between Southeast Asia and Hong Kong persisted through time, this was dependent on virus input from temperate regions and these tropical regions did not maintain a source for annual H3N2 influenza epidemics. We further show that multiple lineages may seed annual influenza epidemics, and that each region may function as a potential source population. We therefore propose that the global persistence of H3N2 influenza A virus is the result of a migrating metapopulation in which multiple different localities may seed seasonal epidemics in temperate regions in a given year. Such complex global migration dynamics may confound control efforts and contribute to the emergence and spread of antigenic variants and drug-resistant viruses.

KW - Evolution

KW - Molecular epidemiology

KW - Phylogeography

KW - Source-sink

UR - http://www.scopus.com/inward/record.url?scp=82755190600&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=82755190600&partnerID=8YFLogxK

U2 - 10.1073/pnas.1109314108

DO - 10.1073/pnas.1109314108

M3 - Article

C2 - 22084096

AN - SCOPUS:82755190600

VL - 108

SP - 19359

EP - 19364

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 48

ER -