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.

The known unknowns of Powassan virus ecology

“…Limited mixing between nearby locations supports the hypothesis that cofeeding transmission from infected nymphs to larvae could be important for DTV maintenance, as small mammalian hosts typically do not move across long distances. Infrequent dispersal of DTV could also provide support for the hypothesis that vertical transmission from adult female to larvae is rare, and does not frequently result in the establishment of new transmission foci (Vogels et al 2023). With adult ticks dispersing over longer distances when feeding on deer, more mixing of DTV would be expected if vertical transmission would play an important role in forming new transmission foci.…”

“…Graphical representation of the knowns and unknowns on the ecology of deer tick virus (DTV; Powassan virus lineage II). Left panel: Illustrative example of the highly focal geographic distribution of DTV, with genomes tightly clustering by location as described in (Vogels et al 2023). Middle panel:The identification of DTV transmission foci raises questions on the size, modes of long-distance dispersal, and frequency of dispersal that remain unanswered.…”

“…Recent phylogenetic studies have significantly increased the DTV genomic dataset and revealed important new insights in the patterns of emergence and spread in the United States (McMinn et al 2023, Vogels et al 2023). Phylogeographic reconstructions revealed that DTV was likely introduced into the Northeast no later than the mid-1970s (Vogels et al 2023). It was estimated that the virus first established in southern parts of New York and Connecticut, followed by emergence towards more northern regions.…”

“…Phylogeographic analyses cannot only provide important insights in the patterns of emergence and spread, but they can also help to understand local transmission dynamics of pathogens. DTV is maintained in highly localized transmission foci with tight clustering by location, and limited mixing between foci in the Northeast (Vogels et al 2023). The isolation between foci is particularly clear in Connecticut, where foci tightly cluster by location and have been stable for over 10 yr (Anderson and Armstrong 2012).…”

“…Novel insights in the geographic distribution of DTV raise important new questions on the ecology of the virus that are relevant to better inform control programs. Although several stable DTV transmission foci have been identified in both the Midwest and Northeast (Brackney et al 2008b, Robich et al 2019, McMinn et al 2023, Vogels et al 2023), it is unclear what size these foci are. Research on TBEV in Europe has suggested that the virus can be maintained in microfoci as small as 250 m 2 (Dobler et al 2011, Weidmann et al 2011, Boelke et al 2019).…”