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to assess global phylogeny of influenza a virus h7 and n9 subtypes , we analyzed 715 hemagglutinin and 309 neuraminidase nucleotide sequences of viruses isolated during 19272012 worldwide ( technical appendix ) .
bayesian markov chain monte carlo coalescent analyses were conducted to investigate recent evolutionary history of influenza a virus h7 and n9 subtypes in eastern asia by using beast version 1.7.4 ( 3,4 ) .
phylogenetic analyses showed maintenance of influenza a virus h7 subtypes in wild birds in eastern asia since 1999 ( clade a ) ( figure 1 , panel a ) .
more specifically , circulation has been restricted mainly to the eastern asia flyway ; most viruses isolated from wild birds were from japan and south korea .
this local perpetuation in wild birds has favored several independent introductions of viruses into poultry in japan , south korea , eastern china ( jiangxi and zhejiang provinces ) , and thailand . a genetically different virus
h7 subtype lineage was detected in europe and asia during 20062012 ( clade b ) ( figure 1 , panel b ) .
these results suggest that 2 influenza a virus h7 subtypes co - circulated in eastern asia during that period . in japan ,
replacement of influenza a virus h7 subtypes that were circulating in wild ducks during 2008 ( clade a ) may have occurred because recent viruses isolated from ducks ( 20112012 ) all belong to clade b. the same pattern was observed in thailand : influenza a virus h7 subtypes isolated in 2011 were genetically different from most viruses isolated in 2010 .
maximum clade credibility trees for co - circulating influenza a virus h7 subtype genetic lineages , eastern asia .
a ) clade a. b ) clade b. values along the branches are posterior probability values > 0.8 .
gray bars indicate 95% highest posterior density for times of the most recent common ancestors ; blue indicates viruses isolated in asia ; green indicates viruses isolated in europe ( details on locations and associated posterior probabilities are shown in the online technical appendix , wwwnc.cdc.gov/eid/article/19/10/13-0609-techapp1.pdf ) ; red indicates a / hangzhou/1/2013(h7n9 ) virus ; and yellow star indicates most recent common ancestral influenza virus among a / hangzhou/1/2013(h7n9 ) virus , zhejiang domestic ducks viruses ( h7n3 ) , and influenza a virus h7 subtype circulating in wild birds .
this pattern suggests that the old genetic lineage of influenza a virus h7 subtypes that circulated in eastern asia since 1999 ( clade a ) may have been progressively replaced by a more recent lineage ( clade b ) .
clustering of clade b viruses with those isolated in europe suggest that gene flow has recently occurred in eurasia , probably as the result of waterfowl migrations and poultry trade .
however , the european origin of viruses from asia was not supported on the basis of phylogeographic analysis ( technical appendix ) .
consistent with results of previous studies ( 1,2,5,6 ) , our results indicate that hemagglutinin of human influenza a(h7n9 ) viruses belongs to clade a and is most genetically related to influenza viruses isolated from domestic ducks at live - poultry markets in zhejiang province , china ( 7 ) .
our findings further indicate that hemagglutinin of human influenza virus did not evolve from the h7 ha circulating in these domestic birds but was derived from a common ancestral influenza a virus circulating in an unidentified host during 2010 . the most recent common ancestral influenza a virus among a / hangzhou/1/2013(h7n9 ) virus , zhejiang domestic duck(h7n3 ) virus , and influenza a virus h7 subtype circulating in wild birds could be dated to 2004 ( figure 1 , panel a ) , indicating that silent introduction and circulation of influenza a virus h7 subtypes in domestic animals might have occurred in this virus before influenza a(h7n9 ) virus was identified in humans ( 8) . limited epidemiologic and genetic information about influenza a virus h7 subtype circulating in eastern china during 20042011 precludes more precise conclusions on origins of human influenza a(h7n9 ) virus and relatedness to influenza a virus circulating in wild birds .
however , on the basis of genetic analyses of recently isolated viruses from chickens , pigeons , and the environment , maintenance and genetic reassortment of emerging influenza a(h7n9 ) virus might have occurred in live poultry markets in shanghai , china ( 5,7 ) .
the phylogenetic structure we observed for influenza a virus subtype n9 suggests that gene flow has occurred since 1996 among europe , africa , asia , and oceania ( figure 2 ; technical appendix ) .
analyses showed circulation of influenza a virus subtype n9 ( mainly h11n9 subtype ) ( figure 2 ) in eastern asia since 2003 , and evidence of virus dispersal to europe and australia and reassortments with hemagglutinin of avian influenza virus subtypes h5 , h6 , and h7 .
consistent with results of other studies ( 1,2,5,6 ) , we found that neuraminidase of a / hangzhou/1/2013(h7n9 ) virus was closely related to that of a / wild bird / korea / a3/2011(h7n9 ) virus ( 9 ) .
however , our estimate of the time of the most recent common ancestral influenza a virus between these 2 viruses was earlier ( 2008 ) than suggested ( 6 ) .
gray bars indicate the 95% highest posterior density for times of the most recent common ancestors .
blue indicates viruses isolated in asia ; green indicates viruses isolated in europe ; purple indicates viruses isolated in oceania ; orange indicates viruses isolated in africa ( details on locations and associated posterior probabilities are shown in the online technical appendix , wwwnc.cdc.gov/eid/article/19/10/13-0609-techapp1.pdf ) ; red indicates a / hangzhou/1/2013(h7n9 ) virus ; and yellow star indicates the basis of influenza a(h11n9 ) virus genetic lineage from asia .
our findings suggest that neuraminidase of human influenza a(h7n9 ) virus might have originated from influenza a(h11n9 ) viruses that circulated in eastern china , although limited information about influenza a virus n9 subtypes circulating in wild birds in this region represents a major challenge to identifying the donor of influenza a(h7n9 ) virus neuraminidase .
reassortments between influenza a(h11n9 ) viruses from asia and influenza a(h1n3 and h7n3 ) viruses circulating in live - poultry markets in zhejiang province were documented in domestic duck in 2011 in nearby jiangsu province ( a / duck / jiangsu/10-d4/2011(h1n3 ) ( 10 ) in a similar fashion , influenza a(h7n9 ) virus could have resulted from silent circulation and reassortment between influenza ( h7n3 and h11n9 ) viruses in live - poultry markets in the shanghai region . as in a study on influenza a virus h7 subtype evolution in wild birds and poultry ( 11 ) , we found no evidence of spillover of influenza a virus h7 subtype from domestic to wild birds and subsequent long - term maintenance in eastern asia .
although we can not formally exclude that local transmission of influenza a virus from domestic to wild birds has occurred , lack of evidence for reintroduction of poultry - adapted viruses into wild birds suggests there has been little to no dissemination of influenza a(h7n9 ) virus by waterfowl along their migratory flyways .
increasing adaptation of this virus to mammals ( 2 ) is unlikely to favor spillover and spread by migratory birds .
however , development and maintenance of influenza a virus surveillance programs for wild waterfowls worldwide are needed to confirm this possibility ( 12,13 ) . in eastern asia ,
2 major influenza a virus h7 subtype genetic lineages have recently circulated in wild and domestic birds , and there has been potential replacement of the older lineage ( clade a ) .
hemagglutinin of influenza a(h7n9 ) virus belongs to clade a. genetic data indicate that the most recent ancestral wild bird  origin virus for a / hangzhou/1/2013(h7n9 ) virus and zhejiang domestic duck viruses can be dated to 2004 .
the influenza a(h11n9 ) virus that circulated in eastern asia for 10 years , with associated intercontinental gene flows and reassortments , may be the donor of influenza a(h7n9 ) virus neuraminidase .
however , influenza a(h7n9 ) virus probably emerged after a long silent circulation in live poultry markets in eastern asia .
global phylogeny of influenza a virus h7 and n9 subtypes and phylogeography of recent h7 and n9 subtype genetic lineages in eastern asia .
influenza a viruses are a threat to poultry and human health . 
 we investigated evolution of influenza a virus h7 and n9 subtypes in wild and domestic birds . 
 influenza a(h7n9 ) virus probably emerged after a long silent circulation in live poultry markets in eastern asia .