Phylogeographic reconstruction of the emergence and spread of Powassan virus in the northeastern United States

Abstract

Powassan virus is an emerging tick-borne virus of concern for public health, but very little is known about its transmission patterns and ecology. Here, we expanded the genomic dataset by sequencing 279 Powassan viruses isolated from Ixodes scapularis ticks from the northeastern United States. Our phylogeographic reconstructions revealed that Powassan virus lineage II was likely introduced or emerged from a relict population in the Northeast between 1940 and 1975. Sequences strongly clustered by sampling location, suggesting a highly focal geographical distribution. Our analyses further indicated that Powassan virus lineage II emerged in the northeastern United States mostly following a south-to-north pattern, with a weighted lineage dispersal velocity of ~3 km/y. Since the emergence in the Northeast, we found an overall increase in the effective population size of Powassan virus lineage II, but with growth stagnating during recent years. The cascading effect of population expansion of white-tailed deer and I. scapularis populations likely facilitated the emergence of Powassan virus in the northeastern United States.

Keywords: Ixodes scapularis; deer tick virus; genomics; tick-borne flavivirus; ticks.

Fig. 1.

Phylogenetic analysis of Powassan virus lineages. (A) Root-to-tip regression performed to assess the temporal signal within the Northeast clade (determination coefficient R² from the linear regression = 0.23). (B) Maximum likelihood tree was obtained from the phylogenetic analysis of publicly available Powassan virus genomes from the United States, Canada, and Russia. Powassan virus lineage II consists of two geographically separated clades in the Northeast and Midwest. Bootstraps support values (based on 1,000 replicates) are provided for the main internal nodes of the tree.

Fig. 2.

Discrete phylogeographic analysis of the dispersal history of Powassan virus in the northeastern United States. (A) MCC tree with branches colored according to the locations inferred at the ancestral nodes. Tip nodes are colored according to their sampling location, and we only displayed internal nodes, using smaller dots and colored according to their inferred location, if they are associated with a posterior probability >0.95. (B) Sampling map and well-supported Markov jumps inferred by discrete phylogeographic inference. Sampling locations are displayed by dots, with the size being proportional to the number of Powassan virus genomic sequences sampled and included in our analyses. We only report Markov jumps associated with an adjusted Bayes factor support higher than three, which corresponds to positive support according to the scale of interpretation as previously defined (22).

Fig. 3.

Spatially explicit phylogeographic analysis of the dispersal history of Powassan virus in the northeastern United States. (A–D) Reconstruction of the dispersal history of Powassan virus lineages inferred by a spatially explicit phylogeographic analysis. We mapped branches of the MCC tree reported in Fig. 2 and whose nodes, as well as associated 80% highest posterior density (HPD) regions, are colored according to their time of occurrence. (E) Skygrid reconstruction of the evolution of the overall effective size of the viral population (Ne). (F) Evolution of the number of confirmed human cases. (G) Estimation of the white-tailed deer (Odocoileus virginianus) populations in the states of New York and Connecticut. (H) Environmental factors included in landscape phylogeographic analyses to test their impact on Powassan virus dispersal.

Fig. 4.

Ixodes scapularis life cycle with proposed hypotheses that may explain the focal distribution of Powassan virus. Life cycle adapted from (41) and created with bioRender.com. Two hypotheses are proposed that may explain the focal distribution of Powassan virus.