Phylogeography and evolutionary history of dengue virus type 3

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Abstract

In this study, we revisited the phylogeography of the three of major DENV-3 genotypes and estimated its rate of evolution, based on the analysis of the envelope (E) gene of 200 strains isolated from 31 different countries around the world over a time period of 50 years (1956–2006). Our phylogenetic analysis revealed a geographical subdivision of DENV-3 population in several country-specific clades. Migration patterns of the main DENV-3 genotypes showed that genotype I was mainly circumspect to the maritime portion of Southeast-Asia and South Pacific, genotype II stayed within continental areas in South-East Asia, while genotype III spread across Asia, East Africa and into the Americas. No evidence for rampant co-circulation of distinct genotypes in a single locality was found, suggesting that some factors, other than geographic proximity, may limit the continual dispersion and reintroduction of new DENV-3 variants. Estimates of the evolutionary rate revealed no significant differences among major DENV-3 genotypes. The mean evolutionary rate of DENV-3 in areas with long-term endemic transmissions (i.e., Indonesia and Thailand) was similar to that observed in the Americas, which have been experiencing a more recent dengue spread. We estimated the origin of DENV-3 virus around 1890, and the emergence of current diversity of main DENV-3 genotypes between the middle 1960s and the middle 1970s, coinciding with human population growth, urbanization, and massive human movement, and with the description of the first cases of DENV-3 hemorrhagic fever in Asia.

Introduction

Dengue virus (DENV) (family Flaviviridae) has a single-stranded positive-sense RNA genome of approximately 11 kb and is transmitted by Aedes aegypti mosquitoes among humans. Infection with DENV may cause an acute “influenza-like” febrile disease called classic dengue fever (DF), or the potentially fatal dengue hemorrhagic fever (DHF) and dengue shock syndrome (DSS). The four known distinct antigenic groups (i.e., serotypes) of DENV (DENV-1 to DENV-4) contain well-defined phylogenetic clusters (i.e., genotypes) that are causing human pandemics. The incidence, geographic distribution and severity of DENV epidemics have dramatically increased since the mid-1950s, probably due to the rapid increase in human population size, uncontrolled urbanization, and the advent of massive human movement which facilitates the spread and proliferation of mosquitoes and infected people (Gubler, 1998, Gubler, 2002, Gubler, 2004, Zanotto et al., 1996). It has been estimated that 50–100 million infections occur annually, and more than 2.5 billion people live in areas of risk for DENV infection (Gubler, 1998, Gubler, 2002, Gubler, 2004).

Using a maximum likelihood framework, Twiddy et al. (2003) extended and re-evaluated the first comprehensive estimates of the rate and time frame of DENV evolution (Zanotto et al., 1996). It was inferred that the current global genetic diversity in the four serotypes of DENV appeared around the last 100 years. Moreover, Twiddy et al. (2003) suggested that all serotypes may be evolving according to a molecular clock; but, for reasons that remain unclear, DENV-3 and the DENV-2 American/Asian genotype had significantly higher substitutions rates when compared to other DENV strains. It has been suggested that under epidemic conditions (i.e., when a new variant is introduced into a susceptible population) the viral transmission rate is higher than under endemic conditions, thus increasing the overall diversity and evolutionary rate of the new variant in the population (Twiddy et al., 2003). A higher evolutionary rate could also be a consequence of the emergence of DENV variants with particular biological properties, such as increased transmissibility, infectiousness, and/or virulence (Cologna and Rico-Hesse, 2003, Holmes and Twiddy, 2003, Messer et al., 2003, Rico-Hesse, 2003, Rico-Hesse et al., 1997). Alternatively, the lineage-specific rate differences in DENV evolution described by Twiddy et al. could be also caused by the low number of sequences used, particularly for DENV-1 (n = 9), DENV-3 (n = 21), and DENV-4 (n = 20) serotypes.

DENV-3 was isolated for the first time during an epidemic outbreak in Philippines in 1956 (Hammon et al., 1960), and since then several DF/DHF outbreaks caused by this serotype have been described world-wide. Five distinct genotypes of DENV-3 have been identified to date (Lanciotti et al., 1994, Wittke et al., 2002). Genotypes I to III (GI to GIII) are responsible for most DENV-3 infections and have been associated with DF/DHF epidemics in Southeast Asia, Indian subcontinent, South Pacific, East Africa, and the Americas. Genotypes IV and V (GIV and GV) were not associated with DHF epidemics and are only represented by a few early sequences from the Americas, South Pacific, and Asia. Many phylogenetic studies on DENV-3 have documented the viral spread within individual countries (Aquino et al., 2006, Chungue et al., 1993, Diaz et al., 2006, Islam et al., 2006, Kobayashi et al., 1999, Peyrefitte et al., 2003, Peyrefitte et al., 2005, Podder et al., 2006, Raekiansyah et al., 2005, Rodriguez-Roche et al., 2005, Usuku et al., 2001, Uzcategui et al., 2003, Wittke et al., 2002, Zhang et al., 2005) or specific regions (Messer et al., 2003), but we still have an incomplete understanding of the global dispersion and evolutionary history of the distinct DENV-3 genotypes.

The objective of the present study was to revise the global phylogeography and evolutionary history of the main DENV-3 genotypes based on the analysis of a large number (n = 200) of envelope (E) gene sequences of DENV-3 strains isolated from 31 different countries around the world over a time period of 50 years (1956–2006).

Section snippets

Sequence datasets

Complete E gene sequences (1479 bp in length) with known date of isolation and representing the full extent of genetic diversity in DENV-3 were collected from GenBank (www.ncbi.nlm.nih.gov). Sequences were excluded from the analysis if they were previously identified as recombinant (Worobey et al., 1999), or were 100% similar to any other strain in the data set. For those genotypes where there were more than 75 sequences available, such as for GII and GIII, a maximum of six sequences randomly

Phylogeography of DENV-3

Our phylogenetic analysis of 200 DENV-3 E gene sequences recovered the five genotypes previously described for this serotype (Lanciotti et al., 1994, Wittke et al., 2002). It also suggested the existence of a strong geographical subdivision of DENV-3 population with no evidences of significant co-circulation of distinct genotypes in a single locality (Fig. 1). Genotype I contained most of the Indonesian strains from 1973 to 2004, along with two early Malaysian isolates (1974 and 1981), one Thai

Discussion

This study represents the largest phylogeographic and evolutionary analysis reported for DENV-3 to date. Our phylogenetic analysis of 200 DENV-3 E sequences with world-wide distribution revealed a clear geographical subdivision of viral strains. Genotypes I, II, and III have been evolving independently in Indonesia, Thailand, and Sri Lanka, respectively, over the last 30–40 years. Our data supports the notion that these countries not only sustain the oldest DENV-3 epidemics but also were

Acknowledgements

This work was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (grant no. 501564/03-9) and FAPERJ (grant no. E-26/152490/2002). We thank Priscila C. Nunes for her technical assistance. J.M.G.A. received fellowship from CNPq. G.B. was funded by a fellowship from the Brazilian FIOCRUZ/CNPq “Pesquisador Visitante” Program.

The authors are grateful for the training they received at the “13th International Bioinformatics Workshop on Virus Evolution and

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