Evolution and expansion dynamics of a vector‐borne virus: 2004–2006 vesicular stomatitis outbreak in the western USA

Abstract

Vesicular stomatitis (VS) is an arthropod-borne viral disease that negatively impacts domestic livestock and wildlife hosts, and economically impacts both private animal owners and the commercial livestock industry. Previous phylogenetic studies, based on partial P gene sequences, suggested that outbreak cycles of the virus (VSV) exhibit a two-phase dynamic (i.e., incursion and expansion). A single viral lineage from endemic areas of Mexico introduced into the southern United States during an incursion year (2004), can overwinter, and then expand throughout the western United States during the subsequent spring and summer seasons (2005). Our objective was to build on this past research using full-length viral genomic sequences from Mexico and the United States from the same outbreak, and a large suite of geospatial data to identify the environmental factors that influence VSV evolution in the United States and potentially drive the incursion-expansion dynamics. Our phylogeographic analysis confirmed that a single VS New Jersey virus (VSNJV) lineage initiated the 2004 incursion year outbreak was subject to decreasing genetic divergence during the 2004-2006 outbreak cycle, and likely overwintered between the 2004-2006 outbreak seasons. However, rather than a simple geographic relationship, viral genetic sublineages or patristic groups identified as part of our study, were found to be associated with seasonally varying evaporative demand, soil moisture, and precipitation. Our results suggest a functional role for these environmental factors in shaping the evolution and ecology of VSNJV. We speculate a nexus to insect-vector switching and possible adaptation to local environmental conditions to help explain the observed incursion-expansion dynamic in the United States in the 2004-2006 outbreak. Our approach of linking the phylogeography of a virus with the ecology of insect vectors can be applied to other vector-borne diseases.

An ensemble learning approach to map the genetic connectivity of the parasitoid Stethynium empoasca (Hymenoptera: Mymaridae) and identify the key influencing environmental and landscape factors

“…Annual precipitation is considered the critical factor, given that it has the highest importance score in both two models. The effect of precipitation on genetic differentiation has been frequently detected in plant and virus species (Avolio et al, 2013;Palinski et al, 2021) but seldom in arthropods (Du et al, 2009;Wellenreuther et al, 2011;French et al, 2022). This could be attributed to some reasons.…”

Vesicular stomatitis Indiana virus near-full-length genome sequences reveal low genetic diversity during the 2019 outbreak in Colorado, USA

“…This cut-off was chosen based on results of a pilot study sequencing a subset of samples with Cts ranging from 16.09 to 33.29. RNA from the original extraction was sequenced in duplicate as previously described ( 14 , 15 ). Briefly, DNA was depleted from extracted samples using the DNA-free DNase kit (Ambion, Austin, TX) following manufacturer's instructions.…”

“…Following incursion into the US, the virus likely overwinters in an as yet unknown host(s) and reemerges to cause outbreaks again the following year ( 1 , 13 ). The virus exhibits different population dynamics during incursion (first year of an outbreak) and expansion [subsequent year(s) of the outbreak] ( 14 ). Outbreaks in the US typically last 1–3 years ( 7 , 10 ).…”

Landscape dynamics of a vector‐borne disease in the westernUS: How vector–habitat relationships inform disease hotspots

“…One risk factor for VS outbreaks in the US is the long‐dispersal distance, often enhanced by high‐wind events, of insect vectors (Burgin et al, 2013; Sellers & Maarouf, 1990). There is strong evidence that overwintering occurs during outbreak cycles in the US (Palinski et al, 2021; Perez et al, 2010). Further studies are needed to determine the mechanisms and specific role of insect vectors during overwintering events.…”

“…Phylogenetic studies indicate that each outbreak cycle in the western US (lasting 1–3 years) is caused by a distinct viral genetic lineage originating in endemic areas in southern Mexico (Rodriguez et al, 2000). The mechanisms of incursion into the US are not fully understood, but studies suggest insect vectors rather than livestock movement are involved (Palinski et al, 2021; Rodrı́guez, 2002). A reservoir host for VSV leading to outbreaks in domestic livestock on the US mainland has not been confirmed; however, feral swine were believed to contribute to the establishment of a VSV‐endemic cycle on Ossabaw Island off the coast of Georgia, USA (Killmaster et al, 2010).…”