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.