Evolution and Expansion Dynamics of a Vector-borne Virus: The 2004-2006 US Vesicular Stomatitis Outbreak in the Western US

Authors: PALINSKI, RACHEL - University Of Kansas; PAUSZEK, STEVEN - Animal And Plant Health Inspection Service (APHIS); Humphreys Jr, John; Peters, Debra; MCVEY, SCOTT - University Of Nebraska; PELZEL-MCCLUSKEY, ANGELA - Animal And Plant Health Inspection Service (APHIS); Derner, Justin; BURRUSS, DYLAN - New Mexico State University; Arzt, Jonathan; Rodriguez, Luis

Submitted to: Ecosphere
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/27/2021
Publication Date: 10/25/2021
Citation: Palinski, R.M., Pauszek, S.J., Humphreys Jr., J.M., Peters, D.C., McVey, S.D., Pelzel-McCluskey, A.M., Derner, J.D., Burruss, D.N., Arzt, J., Rodriguez, L.L. 2021. Evolution and expansion dynamics of a vector-borne virus: 2004-2006 US vesicular stomatitis outbreak in the western USA. Ecosphere. 12(10). Article e03793. https://doi.org/10.1002/ecs2.3793.
DOI: https://doi.org/10.1002/ecs2.3793

Interpretive Summary: Vesicular stomatitis virus (VSV) is an insect-transmitted virus that causes outbreaks of vesicular disease in horses, cattle and pigs. In the western USA outbreaks occur cyclically at approximately 8-10 year intervals. In cattle and pigs the vesicular disease resembles that caused by foot-and-mouth disease virus, a devastating foreign animal disease. The factors mediating the emergence and spread of the virus remain unclear. Previous studies using partial (450 bases) viral genetic sequences, were unable to track the virus distribution and transmission during the 2004-2006 outbreaks. In this study using near full length virus genetic sequences (>10,000 bases) we were able to trace the viral movement from Mexico to southern NM and TX in 2004. Subsequently, in 2005, the virus appeared in 9 states (AZ, CO, ID, MT, NE, NM, TX, UT and WY) and in 2006 VS was detected only in WY. The data analysis suggested that a single VS virus entered the US and caused the 2004 outbreak. this same virus re-emerged in 2005 and 2006. The mechanism of VS emergence and re-emergence remain unclear. However, we found clear associations of specific viruses with environmental conditions. This suggest that different viruses exist in areas with different ecological conditions. Understanding what conditions are necessary for VSV to exist will help device better control methods. Our approach of linking the genetics of a virus with the ecology of insect vectors can be applied to other vector-borne diseases.

Technical 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 US during an incursion year (2004), can overwinter, and then expand throughout the western US during the subsequent spring and summer seasons (2005). Our objective was to build on this past research using new analyses of 60 full-length viral genomic sequences from Mexico and the US for the same outbreak, and a large suite of geospatial data to identify the environmental factors that influence VSV evolution in the US and potentially drive the incursion-expansion dynamic. 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 were identified as part of our study that 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 US in the 2004-2006 outbreak. Our approach of linking the phytogeography of a virus with the ecology of insect vectors can be applied to other vector-borne diseases.