Contrasting landscape epidemiology of two sympatric rabies virus strains

Abstract

Viral strain evolution and disease emergence are influenced by anthropogenic change to the environment. We investigated viral characteristics, host ecology, and landscape features in the rabies-striped skunk disease system of the central Great Plains to determine how these factors interact to influence disease emergence. We amplified portions of the N and G genes of rabies viral RNA from 269 samples extracted from striped skunk brains throughout the distribution of two different rabies strains for which striped skunks were the reservoir. Because the distribution of these two strains overlapped on the landscape and were present in the same host population, we could evaluate how viral properties influenced epidemiological patterns in the area of sympatry. We found that South Central Skunk rabies (SCSK) exhibited intense purifying selection and high infectivity, which are both characteristics of an epizootic virus. Conversely, North Central Skunk rabies (NCSK) exhibited relaxed purifying selection and comparatively lower infectivity, suggesting the presence of an enzootic virus. The host population in the area of sympatry was highly admixed, and skunks among allopatric and sympatric areas had similar effective population sizes. Spatial analysis indicated that landscape features had minimal influence on NCSK movement across the landscape, but those same features were partial barriers to the spread of SCSK. We conclude that NCSK and SCSK have different epidemiological properties that interact differently with both host and landscape features to influence rabies spread in the central Great Plains. We suggest a holistic approach for future studies of emerging infectious diseases that includes studies of viral properties, host characteristics, and spatial features.

The Phylogeography and Spatiotemporal Spread of South-Central Skunk Rabies Virus

“…We demonstrated that SCSK is genetically much more divergent than was inferred previously [3,14]. Evolutionary analysis did not show substantial evidence for positive selection in the dataset.…”

“…Studying patterns of sympatric circulation of SCSK and north-central skunk (NCSK) RABV in the territory of the Great Plains, Barton et al [14] suggested that SCSK may have an increased pathogenicity compared to the NCSK. However, such suggestions should be corroborated via appropriate biological experiments.…”

“…As was suggested, SCSK may exhibit characteristics of an epizootic virus in the Great Plains of North America based on comparative estimates of infectivity and transmissibility obtained from coupling molecular data with landscape features [14]. At least three geographically restricted phylogenetic groups of SCSK were delineated in another study [3].…”

Lack of Genetic Structure and Female-Specific Effect of Dispersal Barriers in a Rabies Vector, the Striped Skunk (Mephitis mephitis)

“…Similar results were obtained in two studies in the USA on this species. No genetic structure was found among groups of skunks in a 61.6 km 2 study area in Texas [76], and a more recent study also failed to find significant genetic population structure over a larger area encompassing parts of North Dakota to Oklahoma (1,250 km 2 , [77]). Altogether, our results and previous evidence suggest a relatively high level of gene flow among groups of skunks which prevents population differentiation over a large scale.…”

Management and modeling approaches for controlling raccoon rabies: The road to elimination

“…One of the most difficult parameters to estimate in pathogen dynamic models is transmission rate, because it depends on knowledge of contact structure among individuals in a population and the relationship between individuals and the virus [97, 39, 38]. Although mapping and other spatial tools have been helpful to understand rabies spread over landscapes, they have limited value in explaining intra-population dynamics and interactions among individuals [29, 98]. Also, conventional compartmental models (e.g., susceptible-infectious-recovered), often assume homogeneous contact structure, but this might not always apply to wildlife populations that have variable degrees of sociality, disease-induced behavioral changes, or other drivers of spatial mixing [99, 29, 39].…”