Article: Phylodynamics of H5N1 avian influenza virus in Indonesia

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TitlePhylodynamics of H5N1 avian influenza virus in Indonesia
AuthorsLam, TTY
Hon, CC
Lemey, P
Pybus, OG
Shi, M
Tun, HM
Li, J
Jiang, J
Holmes, EC
Leung, FCC
Keywordsagriculture
ecology
evolution
influenza
phylodynamics
phylogeography
Issue Date2012
PublisherBlackwell Publishing Ltd. The Journal's web site is located at http://www.blackwellpublishing.com/journals/MEC
CitationMolecular Ecology, 2012, v. 21 n. 12, p. 3062-3077 [How to Cite?]
DOI: http://dx.doi.org/10.1111/j.1365-294X.2012.05577.x
AbstractUnderstanding how pathogens invade and become established in novel host populations is central to the ecology and evolution of infectious disease. Influenza viruses provide unique opportunities to study these processes in nature because of their rapid evolution, extensive surveillance, large data sets and propensity to jump species boundaries. H5N1 highly pathogenic avian influenza virus (HPAIV) is a major animal pathogen and public health threat. The virus is of particular importance in Indonesia, causing severe outbreaks among poultry and sporadic human infections since 2003. However, little is known about how H5N1 HPAIV emerged and established in Indonesia. To address these questions, we analysed Indonesian H5N1 HPAIV gene sequences isolated during 2003-2007. We find that the virus originated from a single introduction into East Java between November 2002 and October 2003. This invasion was characterized by an initially rapid burst of viral genetic diversity followed by a steady rate of lineage replacement and the maintenance of genetic diversity. Several antigenic sites in the haemagglutinin gene were subject to positive selection during the early phase, suggesting that host-immune-driven selection played a role in host adaptation and expansion. Phylogeographic analyses show that after the initial invasion of H5N1, genetic variants moved both eastwards and westwards across Java, possibly involving long-distance transportation by humans. The phylodynamics we uncover share similarities with other recently studied viral invasions, thereby shedding light on the ecological and evolutionary processes that determine disease emergence in a new geographical region. © 2012 Blackwell Publishing Ltd.
ISSN0962-1083
2011 Impact Factor: 5.522
2011 SCImago Journal Rankings: 0.387
DOIhttp://dx.doi.org/10.1111/j.1365-294X.2012.05577.x
ISI Accession Number IDWOS:000304903100021
Funding AgencyGrant Number
Strategic Research Theme of Infection and Immunology, HKU
European Union278433
ERC260864
Newton International Fellowship
Royal Society, UK
Funding Information:

We gratefully thank the Indonesian and other scientists, including those who collected the specimens and sequenced and shared the influenza virus genomes in public sequence databases. We also thank Endang R. Sedyaningsih (MoH, Indonesia) and David Mulyono for useful discussions. We thank Joseph T. Wu (SPH, HKU), the editor and the three anonymous reviewers for important suggestions. The research was supported by funding from the Strategic Research Theme of Infection and Immunology, HKU (to FCL), and the European Union Seventh Framework Programme [FP7/2007-2013] under Grant Agreement no. 278433 and ERC Grant agreement no. 260864 (to PL). TTL is supported by the Newton International Fellowship and both TTL and OGP are supported by Royal Society, UK. We also acknowledge the support of BIOSUPPORT and HPCPOWER projects (HKU) for providing computational resources. We also thank W. K. Kwan and Frankie Cheung for their technical assistance.

ReferencesReferences in Scopus
DC Field
Value
dc.contributor.authorLam, TTY
dc.contributor.authorHon, CC
dc.contributor.authorLemey, P
dc.contributor.authorPybus, OG
dc.contributor.authorShi, M
dc.contributor.authorTun, HM
dc.contributor.authorLi, J
dc.contributor.authorJiang, J
dc.contributor.authorHolmes, EC
dc.contributor.authorLeung, FCC
dc.date.accessioned2012-07-16T09:59:51Z
dc.date.available2012-07-16T09:59:51Z
dc.date.issued2012
dc.description.abstractUnderstanding how pathogens invade and become established in novel host populations is central to the ecology and evolution of infectious disease. Influenza viruses provide unique opportunities to study these processes in nature because of their rapid evolution, extensive surveillance, large data sets and propensity to jump species boundaries. H5N1 highly pathogenic avian influenza virus (HPAIV) is a major animal pathogen and public health threat. The virus is of particular importance in Indonesia, causing severe outbreaks among poultry and sporadic human infections since 2003. However, little is known about how H5N1 HPAIV emerged and established in Indonesia. To address these questions, we analysed Indonesian H5N1 HPAIV gene sequences isolated during 2003-2007. We find that the virus originated from a single introduction into East Java between November 2002 and October 2003. This invasion was characterized by an initially rapid burst of viral genetic diversity followed by a steady rate of lineage replacement and the maintenance of genetic diversity. Several antigenic sites in the haemagglutinin gene were subject to positive selection during the early phase, suggesting that host-immune-driven selection played a role in host adaptation and expansion. Phylogeographic analyses show that after the initial invasion of H5N1, genetic variants moved both eastwards and westwards across Java, possibly involving long-distance transportation by humans. The phylodynamics we uncover share similarities with other recently studied viral invasions, thereby shedding light on the ecological and evolutionary processes that determine disease emergence in a new geographical region. © 2012 Blackwell Publishing Ltd.
dc.description.natureLink_to_subscribed_fulltext
dc.identifier.citationMolecular Ecology, 2012, v. 21 n. 12, p. 3062-3077 [How to Cite?]
DOI: http://dx.doi.org/10.1111/j.1365-294X.2012.05577.x
dc.identifier.doihttp://dx.doi.org/10.1111/j.1365-294X.2012.05577.x
dc.identifier.epage3077
dc.identifier.hkuros200940
dc.identifier.isiWOS:000304903100021
Funding AgencyGrant Number
Strategic Research Theme of Infection and Immunology, HKU
European Union278433
ERC260864
Newton International Fellowship
Royal Society, UK
Funding Information:

We gratefully thank the Indonesian and other scientists, including those who collected the specimens and sequenced and shared the influenza virus genomes in public sequence databases. We also thank Endang R. Sedyaningsih (MoH, Indonesia) and David Mulyono for useful discussions. We thank Joseph T. Wu (SPH, HKU), the editor and the three anonymous reviewers for important suggestions. The research was supported by funding from the Strategic Research Theme of Infection and Immunology, HKU (to FCL), and the European Union Seventh Framework Programme [FP7/2007-2013] under Grant Agreement no. 278433 and ERC Grant agreement no. 260864 (to PL). TTL is supported by the Newton International Fellowship and both TTL and OGP are supported by Royal Society, UK. We also acknowledge the support of BIOSUPPORT and HPCPOWER projects (HKU) for providing computational resources. We also thank W. K. Kwan and Frankie Cheung for their technical assistance.

dc.identifier.issn0962-1083
2011 Impact Factor: 5.522
2011 SCImago Journal Rankings: 0.387
dc.identifier.issue12
dc.identifier.pmid22574738
dc.identifier.scopuseid_2-s2.0-84861998642
dc.identifier.spage3062
dc.identifier.urihttp://hdl.handle.net/10722/153210
dc.identifier.volume21
dc.languageeng
dc.publisherBlackwell Publishing Ltd. The Journal's web site is located at http://www.blackwellpublishing.com/journals/MEC
dc.publisher.placeUnited Kingdom
dc.relation.ispartofMolecular Ecology
dc.relation.referencesReferences in Scopus
dc.rightsThe definitive version is available at www.blackwell-synergy.com
dc.subjectagriculture
dc.subjectecology
dc.subjectevolution
dc.subjectinfluenza
dc.subjectphylodynamics
dc.subjectphylogeography
dc.titlePhylodynamics of H5N1 avian influenza virus in Indonesia
dc.typeArticle
Author Affiliations
  1. Rega Institute for Medical Research
  2. The University of Hong Kong
  3. John E. Fogarty International Center for advanced study in the health sciences
  4. Pennsylvania State University
  5. University of Oxford