The role of neutral and adaptive genomic variation in population diversification and speciation in two ground squirrel species of conservation concern

Understanding the neutral (demographic) and adaptive processes leading to the differentiation of species and populations is a critical component of evolutionary and conservation biology. In this context, recently diverged taxa represent a unique opportunity to study the process of genetic differentiation. Northern and southern Idaho ground squirrels (Urocitellus brunneus – NIDGS, and U. endemicus - SIDGS, respectively) are a recently diverged pair of sister species that have undergone dramatic declines in the last 50 years and are currently found in metapopulations across restricted spatial areas with distinct environmental pressures. Here we genotyped single-nucleotide polymorphisms (SNPs) from buccal swabs with restriction site-associated DNA sequencing (RADseq). With these data we evaluated neutral genetic structure at both the inter- and intra-specific level, and identified putatively adaptive SNPs using population structure outlier and genotype-environment association (GEA) analyses. At the interspecific level, we found a clear separation between NIDGS and SIDGS, and evidence for adaptive differentiation relating to differences in hibernation. At the intraspecific level, we identified 3 Evolutionarily Significant Units for NIDGS and 2 for SIDGS plus multiple Management and Adaptive Units. Elevation appears to be the main driver of adaptive differentiation in NIDGS, while neutral variation patterns match and extend that identified in previous studies using microsatellite markers. For SIDGS, neutral substructure generally reflected the effect of natural geographic barriers, while adaptive variation reflected differences in land cover and temperature. These results clearly highlight the roles of neutral and adaptive processes for understanding species and population differentiation, which can have important conservation implications in threatened species.