Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses.
Dhanasekaran Vijaykrishna1
Justin Bahl
Steven Riley
Lian Duan
Jin Xia Zhang
Honglin Chen
J S Malik Peiris
Gavin J D Smith
Yi Guan
Affiliations1 institutions
State Key Laboratory of Emerging Infectious Diseases, Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Special Administrative Region, China.
The highly pathogenic avian influenza (HPAI) H5N1 virus lineage has undergone extensive genetic reassortment with viruses from different sources to produce numerous H5N1 genotypes, and also developed into multiple genetically distinct sublineages in China. From there, the virus has spread to over 60 countries. The ecological success of this virus in diverse species of both poultry and wild birds with frequent introduction to humans suggests that it is a likely source of the next human pandemic. Therefore, the evolutionary and ecological characteristics of its emergence from wild birds into poultry are of considerable interest. Here, we apply the latest analytical techniques to infer the early evolutionary dynamics of H5N1 virus in the population from which it emerged (wild birds and domestic poultry). By estimating the time of most recent common ancestors of each gene segment, we show that the H5N1 prototype virus was likely introduced from wild birds into poultry as a non-reassortant low pathogenic avian influenza H5N1 virus and was not generated by reassortment in poultry. In contrast, more recent H5N1 genotypes were generated locally in aquatic poultry after the prototype virus (A/goose/Guangdong/1/96) introduction occurred, i.e., they were not a result of additional emergence from wild birds. We show that the H5N1 virus was introduced into Indonesia and Vietnam 3-6 months prior to detection of the first outbreaks in those countries. Population dynamics analyses revealed a rapid increase in the genetic diversity of A/goose/Guangdong/1/96 lineage viruses from mid-1999 to early 2000. Our results suggest that the transmission of reassortant viruses through the mixed poultry population in farms and markets in China has selected HPAI H5N1 viruses that are well adapted to multiple hosts and reduced the interspecies transmission barrier of those viruses.
Biological EvolutionPhylogenyAnimalsBirdsCommunicable Diseases, EmergingGenotypeHumansInfluenza A Virus, H5N1 SubtypePoultrySpecies SpecificityZoonoses
Structured evidence records
Evidence records
9 total
Reservoir Ecology3 records
Reservoir EcologyExtraction confidence 0.90
Key finding
Wild birds acted as the initial ecological source of the H5N1 virus that established and diversified within domestic aquatic poultry populations in China.
The H5N1 prototype virus was likely introduced from wild birds into poultry as a non-reassortant low pathogenic avian influenza H5N1 virus... more recent H5N1 genotypes were generated locally in aquatic poultry after the prototype virus (A/goose/Guangdong/1/96) introduction occurred.
Method
population dynamics analyses
Geographic raw
China
Country inferred
China
Reservoir EcologyExtraction confidence 0.85
Key finding
H5N1 virus spread ecologically from China to poultry populations in Indonesia and Vietnam before outbreak detection, indicating regional transmission dynamics.
The H5N1 prototype virus was likely introduced from wild birds into poultry as a non-reassortant low pathogenic avian influenza H5N1 virus and was not generated by reassortment in poultry.
Method
phylogenetic analysis; genetic analysis
Study design
phylogenetic analysis
Transmission direction
animal-to-animal
Geographic raw
China
Country inferred
China
Cross Species TransmissionExtraction confidence 0.90
Key finding
Reassortant H5N1 viruses were transmitted among mixed poultry species in China, indicating interspecies transmission within poultry populations.
Transmission of reassortant viruses through the mixed poultry population in farms and markets in China has selected HPAI H5N1 viruses that are well adapted to multiple hosts and reduced the interspecies transmission barrier of those viruses.
Method
phylogenetic analysis; population dynamics analysis
Study design
phylogenetic analysis
Transmission direction
animal-to-animal
Geographic raw
China
Country inferred
China
Genomic Evolution1 records
Genomic EvolutionExtraction confidence 0.95
Key finding
Phylogenetic and genomic analysis of H5N1 gene segments showed that the prototype virus originated from wild birds and entered poultry without reassortment.
By estimating the time of most recent common ancestors of each gene segment, we show that the H5N1 prototype virus was likely introduced from wild birds into poultry as a non-reassortant low pathogenic avian influenza H5N1 virus and was not generated by reassortment in poultry.
Reassortant H5N1 influenza viruses selected in mixed poultry populations in China became well adapted to multiple hosts and exhibited reduced interspecies transmission barriers.
Our results suggest that the transmission of reassortant viruses through the mixed poultry population in farms and markets in China has selected HPAI H5N1 viruses that are well adapted to multiple hosts and reduced the interspecies transmission barrier of those viruses.
Mechanism types
host_range; transmission_fitness
Recombination Or Reassortment1 records
Recombination Or ReassortmentExtraction confidence 0.95
Key finding
Reassortant H5N1 viruses generated in aquatic poultry populations in China were selected for multiple-host adaptation, reducing the interspecies transmission barrier.
The highly pathogenic avian influenza (HPAI) H5N1 virus lineage has undergone extensive genetic reassortment with viruses from different sources to produce numerous H5N1 genotypes... Our results suggest that the transmission of reassortant viruses through the mixed poultry population in farms and markets in China has selected HPAI H5N1 viruses that are well adapted to multiple hosts and reduced the interspecies transmission barrier of those viruses.
Event type
reassortment
Spillover Event1 records
Spillover EventExtraction confidence 0.85
Key finding
The H5N1 prototype virus spilled over from wild birds into poultry as a non-reassortant low pathogenic strain.
We show that the H5N1 prototype virus was likely introduced from wild birds into poultry as a non-reassortant low pathogenic avian influenza H5N1 virus.
Method
analytical techniques; phylogenetic inference
Study design
phylogenetic analysis
Transmission direction
unknown
Geographic raw
China
Country inferred
China
Citation context
References
36 references
Reference network
Force-directed citation graph. OmniVira-indexed references are prioritized and recursively expanded up to three steps.
Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong
