Population structure of two rabies hosts relative to the known distribution of rabies virus variants in Alaska

Abstract

For pathogens that infect multiple species the distinction between reservoir hosts and spillover hosts is often difficult. In Alaska, three variants of the arctic rabies virus exist with distinct spatial distributions. We test the hypothesis that rabies virus variant distribution corresponds to the population structure of the primary rabies hosts in Alaska, arctic foxes (Vulpes lagopus) and red foxes (V. vulpes) in order to possibly distinguish reservoir and spill over hosts. We used mitochondrial DNA (mtDNA) sequence and nine microsatellites to assess population structure in those two species. mtDNA structure did not correspond to rabies virus variant structure in either species. Microsatellite analyses gave varying results. Bayesian clustering found 2 groups of arctic foxes in the coastal tundra region, but for red foxes it identified tundra and boreal types. Spatial Bayesian clustering and spatial principal components analysis identified 3 and 4 groups of arctic foxes, respectively, closely matching the distribution of rabies virus variants in the state. Red foxes, conversely, showed eight clusters comprising 2 regions (boreal and tundra) with much admixture. These results run contrary to previous beliefs that arctic fox show no fine-scale spatial population structure. While we cannot rule out that the red fox is part of the maintenance host community for rabies in Alaska, the distribution of virus variants appears to be driven primarily by the artic fox Therefore we show that host population genetics can be utilized to distinguish between maintenance and spillover hosts when used in conjunction with other approaches.

Development of a genotype‐by‐sequencing immunogenetic assay as exemplified by screening for variation in red fox with and without endemic rabies exposure

“…Our dataset partially overlapped the Goldsmith et al. () dataset in having 21 of the same red foxes and six of the same loci (AHT121, AHTh171, CPH9, CPH15, REN105L03, REN247M23). We estimated concordance between the two studies of ~46.7% and noted a large difference in the percent of per‐locus homozygote genotypes between our dataset (1.6%) and the previously published dataset (28.1%; Goldsmith et al., ).…”

“…The AR variants occur on the North Slope (NS; AR variant 3), Seward Peninsula (SP; AR variant 2), and southwestern (SW; AR variant 4) regions of Alaska (Figure ). Conversely, in interior and southcentral (SC) Alaska, only boreal red foxes are found, and AR is not endemic (Goldsmith et al., ). Red fox, a highly susceptible AR host, has been associated with AR spreading from Arctic regions to southern Canada (Kuzmin et al., ).…”

“…Approximate arctic rabies variant ( ARV ) distribution was modified from Goldsmith et al. (). Arctic rabies and arctic rabies‐free zones are indicated by blue and white background colors, respectively.…”

Evolution, ecology and conservation—revisiting three decades of Arctic fox population genetic research

“…Arctic rabies originates from Siberia and it is likely that emigration triggered by lemming crashes in Siberia is the cause underlying rabies outbreaks in Svalbard . In contrast to this, Goldsmith et al (2016) identified divergence of Arctic foxes in a specific region of Alaska, where irregular access to sea ice reduces immigration. Interestingly, the observed genetic structure in this region corresponded to the occurrence of a genetically distinct rabies strain not present elsewhere.…”

Population genetics of fruit bat reservoir informs the dynamics, distribution and diversity of Nipah virus

“…The structure and connectivity of wildlife host populations may influence zoonotic disease dynamics, evolution and spillover risk to people (Biek & Real, ; Cross, Lloyd‐Smith, Johnson, & Getz, ). A better understanding of host population genetic structure will therefore likely improve models of viral circulation dynamics (Goldsmith et al, ; Gryseels et al, ; Guivier et al, ; Rodríguez‐Nevado, Lam, Holmes, & Pagán, ; Streicker et al, ; Wilder, Kunz, & Sorenson, ), but see Fountain‐Jones et al () and Lee et al (). Evolutionary dynamics may also be important in zoonotic emergence, and structuring of host populations has been shown to influence the evolution of pathogen virulence and infectivity (Boots, Hudson, & Sasaki, ; Boots & Mealor, ).…”