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Phylogeography of Japanese encephalitis virus: genotype is associated with climate.

Schuh AJ, Ward MJ, Brown AJ, Barrett AD - PLoS Negl Trop Dis (2013)

Bottom Line: JEV is found throughout most of Asia, extending from maritime Siberia in the north to Australia in the south, and as far as Pakistan to the west and Saipan to the east.We demonstrated that GIII and the recently emerged GI-b are temperate genotypes likely maintained year-round in northern latitudes, while GI-a and GII are tropical genotypes likely maintained primarily through mosquito-avian and mosquito-swine transmission cycles.This study represents a new paradigm directly linking viral molecular evolution and climate.

View Article: PubMed Central - PubMed

Affiliation: Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas, USA.

ABSTRACT
The circulation of vector-borne zoonotic viruses is largely determined by the overlap in the geographical distributions of virus-competent vectors and reservoir hosts. What is less clear are the factors influencing the distribution of virus-specific lineages. Japanese encephalitis virus (JEV) is the most important etiologic agent of epidemic encephalitis worldwide, and is primarily maintained between vertebrate reservoir hosts (avian and swine) and culicine mosquitoes. There are five genotypes of JEV: GI-V. In recent years, GI has displaced GIII as the dominant JEV genotype and GV has re-emerged after almost 60 years of undetected virus circulation. JEV is found throughout most of Asia, extending from maritime Siberia in the north to Australia in the south, and as far as Pakistan to the west and Saipan to the east. Transmission of JEV in temperate zones is epidemic with the majority of cases occurring in summer months, while transmission in tropical zones is endemic and occurs year-round at lower rates. To test the hypothesis that viruses circulating in these two geographical zones are genetically distinct, we applied Bayesian phylogeographic, categorical data analysis and phylogeny-trait association test techniques to the largest JEV dataset compiled to date, representing the envelope (E) gene of 487 isolates collected from 12 countries over 75 years. We demonstrated that GIII and the recently emerged GI-b are temperate genotypes likely maintained year-round in northern latitudes, while GI-a and GII are tropical genotypes likely maintained primarily through mosquito-avian and mosquito-swine transmission cycles. This study represents a new paradigm directly linking viral molecular evolution and climate.

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Related in: MedlinePlus

Climate Bayesian MCC phylogeny of the JEV sequences.GI-V are represented to the right of the tree. Branch tips correspond to the date of collection of each of the virus isolates from which JEV sequence information was derived. Branch lengths correspond to lengths of time (in years), as measured by the scale underneath the tree. Terminal branches are colored according to the sampling location of the taxon at the tip, while internal braches are colored according to the most probable location of their child node. The branch colors correspond to those used in the map and legend. The numbers to the upper-left of the nodes correspond to the country phylogeographic analysis date presented in Table 3 and the numbers to the lower-left of the nodes are posterior probability values.
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pntd-0002411-g004: Climate Bayesian MCC phylogeny of the JEV sequences.GI-V are represented to the right of the tree. Branch tips correspond to the date of collection of each of the virus isolates from which JEV sequence information was derived. Branch lengths correspond to lengths of time (in years), as measured by the scale underneath the tree. Terminal branches are colored according to the sampling location of the taxon at the tip, while internal braches are colored according to the most probable location of their child node. The branch colors correspond to those used in the map and legend. The numbers to the upper-left of the nodes correspond to the country phylogeographic analysis date presented in Table 3 and the numbers to the lower-left of the nodes are posterior probability values.

Mentions: Figures 1 and 2 show the geographical distribution of the JEV sequences included in this study according to the country and climate of collection, respectively. Country and climate Bayesian MCC phylogenies are shown in Figures 3 and 4, respectively. As expected, the topologies of the BEAST phylogenies are supported by the NJ and ML phylogenies (Figures S1 and S2), and are similar to recently published phylogenies generated from both ORF and E gene sequence information for GI-V of the virus [31], [32], [33]. All four of the phylogenies inferred in this study support the division of GI into two clusters, GI-a and GI-b, where the GI-a clade consists of 15 isolates sampled in Cambodia, Thailand and Australia between 1967 and 2005 and GI-b includes 219 isolates sampled from Vietnam, Thailand, Japan, Korea, China and Taiwan between 1979 and 2009. Estimated dates of the MRCA and state PP values in support of each of the 12 countries are presented in Table 2 for the key nodes within the country Bayesian MCC phylogeny (Figure 3), and estimated dates of the MRCA and state PP values in support of tropical and temperate climates of divergence are presented in Table 3 for the key nodes within the climate Bayesian MCC phylogeny (Figure 4).


Phylogeography of Japanese encephalitis virus: genotype is associated with climate.

Schuh AJ, Ward MJ, Brown AJ, Barrett AD - PLoS Negl Trop Dis (2013)

Climate Bayesian MCC phylogeny of the JEV sequences.GI-V are represented to the right of the tree. Branch tips correspond to the date of collection of each of the virus isolates from which JEV sequence information was derived. Branch lengths correspond to lengths of time (in years), as measured by the scale underneath the tree. Terminal branches are colored according to the sampling location of the taxon at the tip, while internal braches are colored according to the most probable location of their child node. The branch colors correspond to those used in the map and legend. The numbers to the upper-left of the nodes correspond to the country phylogeographic analysis date presented in Table 3 and the numbers to the lower-left of the nodes are posterior probability values.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3757071&req=5

pntd-0002411-g004: Climate Bayesian MCC phylogeny of the JEV sequences.GI-V are represented to the right of the tree. Branch tips correspond to the date of collection of each of the virus isolates from which JEV sequence information was derived. Branch lengths correspond to lengths of time (in years), as measured by the scale underneath the tree. Terminal branches are colored according to the sampling location of the taxon at the tip, while internal braches are colored according to the most probable location of their child node. The branch colors correspond to those used in the map and legend. The numbers to the upper-left of the nodes correspond to the country phylogeographic analysis date presented in Table 3 and the numbers to the lower-left of the nodes are posterior probability values.
Mentions: Figures 1 and 2 show the geographical distribution of the JEV sequences included in this study according to the country and climate of collection, respectively. Country and climate Bayesian MCC phylogenies are shown in Figures 3 and 4, respectively. As expected, the topologies of the BEAST phylogenies are supported by the NJ and ML phylogenies (Figures S1 and S2), and are similar to recently published phylogenies generated from both ORF and E gene sequence information for GI-V of the virus [31], [32], [33]. All four of the phylogenies inferred in this study support the division of GI into two clusters, GI-a and GI-b, where the GI-a clade consists of 15 isolates sampled in Cambodia, Thailand and Australia between 1967 and 2005 and GI-b includes 219 isolates sampled from Vietnam, Thailand, Japan, Korea, China and Taiwan between 1979 and 2009. Estimated dates of the MRCA and state PP values in support of each of the 12 countries are presented in Table 2 for the key nodes within the country Bayesian MCC phylogeny (Figure 3), and estimated dates of the MRCA and state PP values in support of tropical and temperate climates of divergence are presented in Table 3 for the key nodes within the climate Bayesian MCC phylogeny (Figure 4).

Bottom Line: JEV is found throughout most of Asia, extending from maritime Siberia in the north to Australia in the south, and as far as Pakistan to the west and Saipan to the east.We demonstrated that GIII and the recently emerged GI-b are temperate genotypes likely maintained year-round in northern latitudes, while GI-a and GII are tropical genotypes likely maintained primarily through mosquito-avian and mosquito-swine transmission cycles.This study represents a new paradigm directly linking viral molecular evolution and climate.

View Article: PubMed Central - PubMed

Affiliation: Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas, USA.

ABSTRACT
The circulation of vector-borne zoonotic viruses is largely determined by the overlap in the geographical distributions of virus-competent vectors and reservoir hosts. What is less clear are the factors influencing the distribution of virus-specific lineages. Japanese encephalitis virus (JEV) is the most important etiologic agent of epidemic encephalitis worldwide, and is primarily maintained between vertebrate reservoir hosts (avian and swine) and culicine mosquitoes. There are five genotypes of JEV: GI-V. In recent years, GI has displaced GIII as the dominant JEV genotype and GV has re-emerged after almost 60 years of undetected virus circulation. JEV is found throughout most of Asia, extending from maritime Siberia in the north to Australia in the south, and as far as Pakistan to the west and Saipan to the east. Transmission of JEV in temperate zones is epidemic with the majority of cases occurring in summer months, while transmission in tropical zones is endemic and occurs year-round at lower rates. To test the hypothesis that viruses circulating in these two geographical zones are genetically distinct, we applied Bayesian phylogeographic, categorical data analysis and phylogeny-trait association test techniques to the largest JEV dataset compiled to date, representing the envelope (E) gene of 487 isolates collected from 12 countries over 75 years. We demonstrated that GIII and the recently emerged GI-b are temperate genotypes likely maintained year-round in northern latitudes, while GI-a and GII are tropical genotypes likely maintained primarily through mosquito-avian and mosquito-swine transmission cycles. This study represents a new paradigm directly linking viral molecular evolution and climate.

Show MeSH
Related in: MedlinePlus