The role of a mechanistic host in maintaining arctic rabies variant distributions: Assessment of functional genetic diversity in Alaskan red fox (Vulpes vulpes).

Tristan M Baecklund,Michael E Donaldson,Jaycee Morrison,Christopher J Kyle,Karsten Hueffer,Hoh Boon-Peng

doi:10.1371/journal.pone.0249176

Abstract

Populations are exposed to different types and strains of pathogens across heterogeneous landscapes, where local interactions between host and pathogen may present reciprocal selective forces leading to correlated patterns of spatial genetic structure. Understanding these coevolutionary patterns provides insight into mechanisms of disease spread and maintenance. Arctic rabies (AR) is a lethal disease with viral variants that occupy distinct geographic distributions across North America and Europe. Red fox (Vulpes vulpes) are a highly susceptible AR host, whose range overlaps both geographically distinct AR strains and regions where AR is absent. It is unclear if genetic structure exists among red fox populations relative to the presence/absence of AR or the spatial distribution of AR variants. Acquiring these data may enhance our understanding of the role of red fox in AR maintenance/spread and inform disease control strategies. Using a genotyping-by-sequencing assay targeting 116 genomic regions of immunogenetic relevance, we screened for sequence variation among red fox populations from Alaska and an outgroup from Ontario, including areas with different AR variants, and regions where the disease was absent. Presumed neutral SNP data from the assay found negligible levels of neutral genetic structure among Alaskan populations. The immunogenetically-associated data identified 30 outlier SNPs supporting weak to moderate genetic structure between regions with and without AR in Alaska. The outliers included SNPs with the potential to cause missense mutations within several toll-like receptor genes that have been associated with AR outcome. In contrast, there was a lack of genetic structure between regions with different AR variants. Combined, we interpret these data to suggest red fox populations respond differently to the presence of AR, but not AR variants. This research increases our understanding of AR dynamics in the Arctic, where host/disease patterns are undergoing flux in a rapidly changing Arctic landscape, including the continued northward expansion of red fox into regions previously predominated by the arctic fox (Vulpes lagopus).

Highlights

Understanding patterns of local adaptation is important to enhance insights into how species interact with their environment, and in clarifying how rapid changes in the suite of selective pressures influence population fitness and persistence [1,2]
The combined dataset (N = 125) of newly (n = 96) and previously (n = 29) sequenced samples had an average of ~315,000 raw reads per library, of which 96.2% mapped to the canine reference genome, ~11.6% reads were filtered per library, and ~58% aligned to targeted regions (~ 65X coverage; S3 Table)
Analyses containing only the Alaskan samples provided results similar to those obtained when we analyzed the subset of data containing red fox populations from both Alaska and Ontario; where Principle component analysis (PCA) and discriminant analyses of principle components (DAPC) analyses identified no population genetic structure within Alaska, STRUCTURE results were suggestive of weak patterns of substructure (S1 Fig)

Summary

Introduction

Understanding patterns of local adaptation is important to enhance insights into how species interact with their environment, and in clarifying how rapid changes in the suite of selective pressures influence population fitness and persistence [1,2]. The process of local adaptation is influenced by selective pressures and the interplay of gene flow and effective population size (genetic drift) relative to the strength of the selective pressure. Gene flow and genetic drift undermine a population’s ability to locally adapt through either the homogenization of genetic variation or through the random loss of genetic variants in small populations [1,5]. If selection is both divergent in nature, and stronger than the combined force of gene flow and genetic drift, local adaptation is likely to occur [1]. Short of common garden experiments which can be difficult to undertake in natural systems, genetic assessments of the interactions between selection and the demographic forces acting on different populations provide a means to detect patterns indicative of local adaptation. Genetic signals of locally adapted populations have been identified across a wide range of systems including nonsynonymous gene changes among wolf populations that correlate with precipitation and vegetation patterns [8], and variation in salmonid immune genes associated with the thermal regimes of different waterbodies [9]

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