Multi-year evolutionary dynamics of West Nile virus in suburban Chicago, USA, 2005-2007

Abstract

West Nile virus has evolved in concert with its expansion across North America, but little is known about the evolutionary dynamics of the virus on local scales. We analysed viral nucleotide sequences from mosquitoes collected in 2005, 2006, and 2007 from a known transmission 'hot spot' in suburban Chicago, USA. Within this approximately 11 x 14 km area, the viral envelope gene has increased approximately 0.1% yr(-1) in nucleotide-level genetic diversity. In each year, viral diversity was higher in 'residential' sites characterized by dense housing than in more open 'urban green space' sites such as cemeteries and parks. Phylodynamic analyses showed an increase in incidence around 2005, consistent with a higher-than-average peak in mosquito and human infection rates that year. Analyses of times to most recent common ancestor suggest that WNV in 2005 and 2006 may have arisen predominantly from viruses present during 2004 and 2005, respectively, but that WNV in 2007 had an older common ancestor, perhaps indicating a predominantly mixed or exogenous origin. These results show that the population of WNV in suburban Chicago is an admixture of viruses that are both locally derived and introduced from elsewhere, containing evolutionary information aggregated across a breadth of spatial and temporal scales.

Figure 1.

Phylogenetic tree constructed using Bayesian analysis of 254 WNV envelope gene sequences (length 1575 nucleotides) from suburban Chicago, plus eight out-group sequences. Taxon names generated from the Chicago study area indicate collection site (described in Bertolotti et al. 2008), identification number (only for WNV sequences from mosquitoes collected in 2005), dates of collection (YearMonthDay for sequences from mosquitoes collected in 2006 and 2007), and GenBank accession numbers (in parentheses). Posterior probabilities of clades are indicated above branches.

Figure 2.

WNV genetic diversity in Culex mosquitoes from suburban Chicago, 2005–2007. Genetic diversity is expressed as nucleotide diversity (Nei 1987), or mean proportion of nucleotide differences among sequences within each year, corrected for multiple substitutions using a model of molecular evolution derived from a hierarchical likelihood ratio test approach implemented using the computer program Modeltest, v. 3.7 (Posada & Crandall 2001). Lines and small error bars indicate means and standard errors, respectively. Boxes indicate third quartiles, and large error bars indicate ranges. The dashed line is a least squares regression line indicating the rate of increase of viral genetic diversity over time (0.94 × 10⁻³ yr⁻¹, R² = 0.32, t = 36.8, p < 0.01). Grey lines are least-squares regression lines derived from 1000 bootstrap replicates of the data; solid lines indicate 95% CI around the nucleotide diversity estimation. Sample sizes for each year are indicated in parentheses.

Figure 3.

Bayesian skyline plot of WNV in suburban Chicago, USA. The black bold dashed line represents the median estimate of effective number of infections through time in suburban Chicago, derived from ENV gene sequences using a Bayesian coalescent approach. Genetic distances were transformed into a time scale of days taking into account the different sampling times of WNV in our study area and enforcing a relaxed molecular clock (see §2). Ninety-five per cent HPD values shaded. Vertical dashed grey lines indicate the sampling periods (21 July–4 October 2005, 13 June–7 Septmber 2006, 5 July–9 September 2007) for the WNV sequences analysed in this study.