Evidence of Intraspecific Adaptive Variation in the American Pika (Ochotona princeps) on a Continental Scale Using a Target Enrichment and Mitochondrial Genome Skimming Approach

Abstract

Montane landscapes present an array of abiotic challenges that drive adaptive evolution amongst organisms. These adaptations can promote habitat specialisation, which may heighten the risk of extirpation from environmental change. For example, higher metabolic rates in an endothermic species may contribute to heightened cold tolerance, whilst simultaneously limiting heat tolerance. Here, using the climate-sensitive American pika (Ochotona princeps), we test for evidence of intraspecific adaptive variation amongst environmental gradients across the Intermountain West of North America. We leveraged results from previous studies on pika adaptation to generate a custom nuclear target enrichment design to sequence several hundred candidate genes related to cold, hypoxia and dietary detoxification. We also applied a 'genome skimming' approach to sequence mitochondrial DNA. Using genotype-environment association tests, we identified rare genomic variants associated with elevation and temperature variation amongst populations. Amongst mitochondrial genes, we identified intraspecific variation in selective signals and significant changes to the amino acid property equilibrium constant, which may relate to electron transport chain efficiency. These results illustrate a complex dynamic of adaptive variation amongst O. princeps where lineages and populations have adapted to unique regional conditions. Some of the clearest signals of selection were in a genetic lineage that includes pikas of the Great Basin region, which is also where recent localised extirpations have taken place and highlights the risk of losing adaptive alleles during environmental change.

Keywords: abiotic adaptation; climate change; genotype–environment association; high‐elevation; landscape genomics; population genetics.

FIGURE 1

Sampling localities of Ochotona princeps used for this study, coloured by subspecies and with point size corresponding to site elevation. Shaded regions are meant to serve as visual aids in illustrating results from Galbreath et al. (2010), as they also encompass regions unsuitable for pikas. Official subspecies names and abbreviations are as follows: O. p. princeps (Northern Rocky Mountains; NRM), O. p. fenisex (Coast Mountains and Cascade Range; CR), O. p. saxatilis (Southern Rocky Mountains; SRM), O. p. schisticeps (Sierra Nevada and Great Basin; SN), and O. p. uinta (Uinta Mountains and Wasatch Range; CU) (Galbreath, Hafner, and Zamudio ; Galbreath et al. ; Hafner and Smith 2010).

FIGURE 2

Nuclear SNPs grouped by six O. princeps lineages. (A) PCA of nuclear SNPs where each point is a sample coloured by one of six O. princeps lineages, calculated with snmf. (B) map of sampling locations used for this study separated by our snmf results.

FIGURE 3

Significant loci identified from LFMM categorised by O. princeps lineage. (A) PCA of intersecting significant loci (34) from LFMM ridge and LFMM lasso models, with star marking samples from the Mud Lake locality of the Sierra Nevada lineage. (B) Map of six O. princeps lineages, noting the outlier population (Sierra Nevada – Mud Lake; denoted by a star) with the greatest separation on Axis 1 of PCA.

FIGURE 4

RDA results from six O. princeps lineages with environmental predictors mean coldest month temperature (MCMT) and elevation. (A) Results from RDA1 and RDA2, show all SNPs as points in the center of the plot, each sample as a point coloured by its lineage and vectors of the two environmental predictors. (B) Results from RDA1 and RDA2 with points representing individual SNPs where grey is neutral, red is a significant outlier SNP most influenced by elevation and teal is a significant outlier SNP most influenced by MCMT.

FIGURE 5

Genotype PCA of SNPs under diversifying selection in BayeScan. All samples in the SNP dataset are represented as points coloured by O. princeps lineage. Note that all NRM‐NW and NRM‐SE samples cover the same space.

FIGURE 6

Significant changes in pK′ of mitochondrial protein‐coding genes of six O. princeps snmf lineages. (A) Linear regression of the sum of the change in pK′ by elevation in meters (p=2.87e‐6) and (B) linear regression of the sum of the change in pK′ by mean coldest month temperature in Celsius (p=0.028), shapes and colours correspond to O. princeps snmf lineage. (C) Average change in pK′ of mitochondrial protein‐coding genes for the six O. princeps snmf lineages.