Movement of St. Louis encephalitis virus in the Western United States, 2014- 2018

Abstract

St. Louis encephalitis virus (SLEV) is a flavivirus that circulates in an enzootic cycle between birds and mosquitoes and can also infect humans to cause febrile disease and sometimes encephalitis. Although SLEV is endemic to the United States, no activity was detected in California during the years 2004 through 2014, despite continuous surveillance in mosquitoes and sentinel chickens. In 2015, SLEV-positive mosquito pools were detected in Maricopa County, Arizona, concurrent with an outbreak of human SLEV disease. SLEV-positive mosquito pools were also detected in southeastern California and Nevada in summer 2015. From 2016 to 2018, SLEV was detected in mosquito pools throughout southern and central California, Oregon, Idaho, and Texas. To understand genetic relatedness and geographic dispersal of SLEV in the western United States since 2015, we sequenced four historical genomes (3 from California and 1 from Louisiana) and 26 contemporary SLEV genomes from mosquito pools from locations across the western US. Bayesian phylogeographic approaches were then applied to map the recent spread of SLEV. Three routes of SLEV dispersal in the western United States were identified: Arizona to southern California, Arizona to Central California, and Arizona to all locations east of the Sierra Nevada mountains. Given the topography of the Western United States, these routes may have been limited by mountain ranges that influence the movement of avian reservoirs and mosquito vectors, which probably represents the primary mechanism of SLEV dispersal. Our analysis detected repeated SLEV introductions from Arizona into southern California and limited evidence of year-to-year persistence of genomes of the same ancestry. By contrast, genetic tracing suggests that all SLEV activity since 2015 in central California is the result of a single persistent SLEV introduction. The identification of natural barriers that influence SLEV dispersal enhances our understanding of arbovirus ecology in the western United States and may also support regional public health agencies in implementing more targeted vector mitigation efforts to protect their communities more effectively.

Fig 1

(A): Map of the Americas showing the distribution of genotype III St. Louis encephalitis virus genomes used in this study (circles). The 40°N latitude line is shown by a blue hatched line. The varied landscape of the Western US is shown, including (B) elevation with several mountain ranges highlighted and annual mean temperature (C).

Fig 2. Maximum Likelihood phylogenetic tree highlighting the evolutionary history of SLEV genotype III in the Western US.

SLEV genomes comprising all genotypes (A) or genotype III only (B) are shown. Genomes in red were sequenced for this study. For panel A, branch colors denote genotypes represented by the key. For both A and B, the percentage of trees in which the associated genomes clustered together is indicated by the colored circles at nodes with pink indicating high support (1) and brown indicating low support (0). Branch length is scaled to reflect the number of substitutions per site. The branch length scale for both trees is provided under the tree in B. Genomes are named as follows: Strain_Location_Year. Abbreviations: Argentina, ARG; Arizona AZ; Brazil, BRA; California, CA; Colorado, CO; Florida, FL; Guatemala, GTM; Haiti, HTI; Idaho ID; Kentucky, KY; Louisiana, LA; Mexico, MEX; Mississippi, MS; Missouri, MO; Nevada, NV; Oregon, OR; Panama, PAN; Peru, PER; Tennessee, TN; Texas, TX, Trinidad and Tobago, TTO.

Fig 3. Bayesian phylogeographic analysis showing four distinct clusters of SLEV genotype III in the western US.

The branch length is scaled to time in years and the posterior support of each node is represented by the colored circle. Branch length scale is provided at the base of the phylogeny. Colored stars to the left of clades denote shared amino acid substitutions: Black = A-261-V, G-2195-S, L-2210-S, and A-2383-V; Red = G-2288-E; Green = H1079-I and I-2233-V; Blue = I-3095-V; Dark purple = P-2298-S and Light purple = Q-538-R. The map indicates the location of mosquito pool collections. Circles represent new genomes that were generated during this study and triangles represent old genomes sourced from GenBank. Genome names are as follows: Strain_Location_Year. Abbreviations: Argentina, ARG; Arizona, AZ; California, CA; Idaho, ID; Nevada, NV; Oregon, OR; Texas, TX.

Fig 4. Geographic expansion of SLEV genotype III likely followed three routes throughout the Western US.

Genomes and inferred ancestors are represented with blue circles. The inferred SLEV expansion is depicted for each year for 2014–2017 and a composite is shown for 2014–2018. Route one, shown by a red arrow, consists of SLEV expansion from AZ into Southern CA. Route two, circled in purple, involves SLEV transported from AZ into the Central Valley of CA. Route three, indicated with a green bracket, represents SLEV movement from AZ to all locations east of the Sierra Nevada mountains.