Bayesian phylodynamics of avian influenza A virus H9N2 in Asia with time-dependent predictors of migration

Model-based phylodynamic approaches recently employed generalized linear models (GLMs) to uncover potential predictors of viral spread. Very recently some of these models have allowed both the predictors and their coefficients to be time-dependent. However, these studies mainly focused on predictors that are assumed to be constant through time. Here we inferred the phylodynamics of avian influenza A virus H9N2 isolated in 12 Asian countries and regions under both discrete trait analysis (DTA) and structured coalescent (MASCOT) approaches. Using MASCOT we applied a new time-dependent GLM to uncover the underlying factors behind H9N2 spread. We curated a rich set of time-series predictors including annual international live poultry trade and national poultry production figures. This time-dependent phylodynamic prediction model was compared to commonly employed time-independent alternatives. Additionally the time-dependent MASCOT model allowed for the estimation of viral effective sub-population sizes and their changes through time, and these effective population dynamics within each country were predicted by a GLM. International annual poultry trade is a strongly supported predictor of virus migration rates. There was also strong support for geographic proximity as a predictor of migration rate in all GLMs investigated. In time-dependent MASCOT models, national poultry production was also identified as a predictor of virus genetic diversity through time and this signal was obvious in mainland China. Our application of a recently introduced time-dependent GLM predictors integrated rich time-series data in Bayesian phylodynamic prediction. We demonstrated the contribution of poultry trade and geographic proximity (potentially unheralded wild bird movements) to avian influenza spread in Asia. To gain a better understanding of the drivers of H9N2 spread, we suggest increased surveillance of the H9N2 virus in countries that are currently under-sampled as well as in wild bird populations in the most affected countries.

[1]  Remco Bouckaert,et al.  Coupled MCMC in BEAST 2 , 2019 .

[2]  D. Cummings,et al.  Understanding dengue virus evolution to support epidemic surveillance and counter-measure development. , 2018, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[3]  M. Gilbert,et al.  Predictive gravity models of livestock mobility in Mauritania: The effects of supply, demand and cultural factors , 2018, PloS one.

[4]  P. Lemey,et al.  On the importance of negative controls in viral landscape phylogeography , 2018, Virus evolution.

[5]  S. Lycett,et al.  Circulation of Foot-and-Mouth Disease Virus in Africa and identification of the underlying constraints using Phylogeographic methods , 2018 .

[6]  Tanja Stadler,et al.  Inferring time-dependent migration and coalescence patterns from genetic sequence and predictor data in structured populations , 2018, bioRxiv.

[7]  M. Suchard,et al.  Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7 , 2018, Systematic biology.

[8]  O. Demin,et al.  Correction: A mathematical model of multisite phosphorylation of tau protein , 2018, PloS one.

[9]  Daniel L. Ayres,et al.  Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10 , 2018, Virus evolution.

[10]  S. Lim,et al.  Prevalence of avian influenza (H9N2) in commercial quail, partridge, and turkey farms in Iran, 2014–2015 , 2018, Tropical Animal Health and Production.

[11]  Junjie Yue,et al.  Genetic Characteristic and Global Transmission of Influenza A H9N2 Virus , 2017, Front. Microbiol..

[12]  G. Dong,et al.  Journey to the east: Diverse routes and variable flowering times for wheat and barley en route to prehistoric China , 2017, PloS one.

[13]  Matthias Bethge,et al.  Signatures of criticality arise from random subsampling in simple population models , 2016, PLoS Comput. Biol..

[14]  Xiufan Liu,et al.  Current situation of H9N2 subtype avian influenza in China , 2017, Veterinary Research.

[15]  Tanja Stadler,et al.  MASCOT: parameter and state inference under the marginal structured coalescent approximation , 2017, bioRxiv.

[16]  R. Gao,et al.  A comprehensive retrospective study of the seroprevalence of H9N2 avian influenza viruses in occupationally exposed populations in China , 2017, PloS one.

[17]  Trevor Bedford,et al.  Virus genomes reveal factors that spread and sustained the Ebola epidemic , 2017, Nature.

[18]  Anthony J. Geneva,et al.  RWTY (R We There Yet): An R Package for Examining Convergence of Bayesian Phylogenetic Analyses. , 2017, Molecular biology and evolution.

[19]  Matthew Scotch,et al.  Bayesian phylogeography of influenza A/H3N2 for the 2014-15 season in the United States using three frameworks of ancestral state reconstruction , 2017, PLoS Comput. Biol..

[20]  David K. Smith,et al.  ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data , 2017 .

[21]  Tanja Stadler,et al.  The Structured Coalescent and Its Approximations , 2016, bioRxiv.

[22]  Thomas P. Fabrizio,et al.  Prevalence and diversity of H9N2 avian influenza in chickens of Northern Vietnam, 2014 , 2016, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[23]  Manuel Llinás,et al.  Open Source Drug Discovery with the Malaria Box Compound Collection for Neglected Diseases and Beyond , 2016, PLoS pathogens.

[24]  Eric J. Ma,et al.  Ecosystem Interactions Underlie the Spread of Avian Influenza A Viruses with Pandemic Potential , 2016, PLoS pathogens.

[25]  R. Webster,et al.  The replication of Bangladeshi H9N2 avian influenza viruses carrying genes from H7N3 in mammals , 2016, Emerging Microbes & Infections.

[26]  Andrew Rambaut,et al.  Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen) , 2016, Virus evolution.

[27]  Guy Baele,et al.  Bayesian Inference Reveals Host-Specific Contributions to the Epidemic Expansion of Influenza A H5N1. , 2015, Molecular biology and evolution.

[28]  Remco R. Bouckaert,et al.  Bayesian Evolutionary Analysis with BEAST , 2015 .

[29]  Tanya M. Teslovich,et al.  The Influence of Age and Sex on Genetic Associations with Adult Body Size and Shape: A Large-Scale Genome-Wide Interaction Study , 2015, PLoS Genetics.

[30]  Nicola De Maio,et al.  New Routes to Phylogeography: A Bayesian Structured Coalescent Approximation , 2015, PLoS genetics.

[31]  M. Killian,et al.  Novel Eurasian Highly Pathogenic Avian Influenza A H5 Viruses in Wild Birds, Washington, USA, 2014 , 2015, Emerging infectious diseases.

[32]  M. Killian,et al.  Novel Eurasian Highly Pathogenic Avian Influenza A H 5 Viruses in Wild Birds , 2015 .

[33]  Baoli Zhu,et al.  Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus , 2014, Proceedings of the National Academy of Sciences.

[34]  M. Iqbal,et al.  A global phylogenetic analysis in order to determine the host species and geography dependent features present in the evolution of avian H9N2 influenza hemagglutinin , 2014, PeerJ.

[35]  Sarah A. Butcher,et al.  Hydrophobin Film Structure for HFBI and HFBII and Mechanism for Accelerated Film Formation , 2014, PLoS Comput. Biol..

[36]  R. Gao,et al.  Genesis of the novel human-infecting influenza A(H10N8) virus and potential genetic diversity of the virus in poultry, China. , 2014, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[37]  David Welch,et al.  Efficient Bayesian inference under the structured coalescent , 2014, Bioinform..

[38]  G. Gao,et al.  Influenza and the Live Poultry Trade , 2014, Science.

[39]  Dong Xie,et al.  BEAST 2: A Software Platform for Bayesian Evolutionary Analysis , 2014, PLoS Comput. Biol..

[40]  M. Suchard,et al.  Unifying Viral Genetics and Human Transportation Data to Predict the Global Transmission Dynamics of Human Influenza H3N2 , 2014, PLoS pathogens.

[41]  R. Webster,et al.  Genesis of avian influenza H9N2 in Bangladesh , 2014, Emerging Microbes & Infections.

[42]  Guy Baele,et al.  Inferring Heterogeneous Evolutionary Processes Through Time: from Sequence Substitution to Phylogeography , 2013, Systematic biology.

[43]  Yu Wang,et al.  Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses , 2013, The Lancet.

[44]  Marc A Suchard,et al.  Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[46]  E. Khamas Avian Influenza ( H 9 N 2 ) Outbreak In Iraq , 2012 .

[47]  Walter Zucchini,et al.  Model Selection , 2011, International Encyclopedia of Statistical Science.

[48]  D. Douglas,et al.  Potential spread of highly pathogenic avian influenza H5N1 by wildfowl: dispersal ranges and rates determined from large-scale satellite telemetry , 2010 .

[49]  Alexei J. Drummond,et al.  Bayesian Phylogeography Finds Its Roots , 2009, PLoS Comput. Biol..

[50]  C. Davis,et al.  Characterization of a highly pathogenic avian influenza H5N1 virus sublineage in poultry seized at ports of entry into Vietnam. , 2009, Virology.

[51]  T. Kuiken,et al.  Wild Ducks as Long-Distance Vectors of Highly Pathogenic Avian Influenza Virus (H5N1) , 2008, Emerging infectious diseases.

[52]  Tony O’Hagan Bayes factors , 2006 .

[53]  K. Tsukamoto,et al.  Characterization of H9N2 influenza A viruses isolated from chicken products imported into Japan from China , 2006, Epidemiology and Infection.

[54]  Y. Kawaoka,et al.  Properties and Dissemination of H5N1 Viruses Isolated during an Influenza Outbreak in Migratory Waterfowl in Western China , 2006, Journal of Virology.

[55]  A. Osterhaus,et al.  Global Patterns of Influenza A Virus in Wild Birds , 2006, Science.

[56]  G. Gao,et al.  Highly Pathogenic H5N1 Influenza Virus Infection in Migratory Birds , 2005, Science.

[57]  R. Webster,et al.  Avian influenza viruses in Korean live poultry markets and their pathogenic potential. , 2005, Virology.

[58]  J. Felsenstein Evolutionary trees from DNA sequences: A maximum likelihood approach , 2005, Journal of Molecular Evolution.

[59]  K. Asasi,et al.  Avian Influenza (H9N2) Outbreak in Iran , 2003, Avian diseases.

[60]  M. Suchard,et al.  Bayesian selection of continuous-time Markov chain evolutionary models. , 2001, Molecular biology and evolution.

[61]  Edward I. George,et al.  The Practical Implementation of Bayesian Model Selection , 2001 .

[62]  I. Brown,et al.  H9N2 subtype influenza A viruses in poultry in pakistan are closely related to the H9N2 viruses responsible for human infection in Hong Kong. , 2000, Virology.

[63]  Y. Guan,et al.  Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. , 2000, Virology.

[64]  Y. Guan,et al.  Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[65]  N. Takahata,et al.  The coalescent in two partially isolated diffusion populations. , 1988, Genetical research.