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 intraspecific
level, and identified putatively adaptive SNPs using population structure
outlier detection and genotype-environment association (GEA) analyses. At
the interspecific level, we detected a clear separation between NIDGS and
SIDGS, and evidence for adaptive differentiation putatively linked to
torpor patterns. At the intraspecific level, we found evidence of both
neutral and adaptive differentiation. For NIDGS, elevation appears to be
the main driver of adaptive differentiation, while neutral variation
patterns match and expand information on the low connectivity between some
populations identified in previous studies using microsatellite markers.
For SIDGS, neutral substructure generally reflected natural geographic
barriers, while adaptive variation reflected differences in land cover and
temperature, as well as elevation. These results clearly highlight the
roles of neutral and adaptive processes for understanding the complexity
of the processes leading to species and population differentiation, which
can have important conservation implications in susceptible and threatened
species.