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