Integrative species delimitation reveals an Idaho-endemic ground squirrel, Urocitellus idahoensis (Merriam 1913)

Abstract

The "small-eared" species group of Urocitellus ground squirrels (Sciuridae: Xerinae: Marmotini) is endemic to the Great Basin, United States, and surrounding cold desert ecosystems. Most specific and subspecific lineages in this group occupy narrow geographic ranges, and some are of significant conservation concern; despite this, current taxonomy remains largely based on karyotypic or subtle pelage and morphological characteristics. Here, we leverage 2 multilocus DNA sequence data sets and apply formal species delimitation tests alongside morphometric comparisons to demonstrate that the most widespread small-eared species (U. mollis Kennicott, 1863 sensu lato; Piute Ground Squirrel) is comprised of 2 nonsister and deeply divergent lineages. The 2 lineages are geographically separated by the east-west flowing Snake River in southern Idaho, with no sites of sympatry currently known. Based on robust support across the nuclear genome, we elevate populations previously attributed to U. mollis from north of the Snake River to species status under the name Urocitellus idahoensis (Merriam 1913) and propose the common name "Snake River Plains Ground Squirrel" for this taxon. We delimit 2 subspecies within U. idahoensis; U. i. idahoensis (Merriam 1913) in western Idaho and U. i. artemesiae (Merriam 1913) in eastern Idaho. Urocitellus idahoensis is endemic to Idaho and has a maximal range area of roughly 29,700 km² spanning 22 counties but occurs discontinuously across this area. Our work substantially expands knowledge of ground squirrel diversity in the northern Great Basin and Columbia Plateau and highlights the difficulty in delimiting aridland mammals whose morphological attributes are highly conserved.

Keywords: Columbia Plateau; Great Basin; Marmotini; Snake River; UCEs; geometric morphometrics; mitonuclear discordance.

Fig. 1.

Map of the western United States depicting geographic ranges of subspecies of Urocitellus mollis. The Snake River in Idaho delimits the northern range limit of U. m. mollis and the southern range limits of U. m. idahoensis and U. m. artemesiae, and stippling represents the presumed boundary of the latter 2 subspecies.

Fig. 2.

Maximum clade credibility (MCC) phylograms of small-eared Urocitellus inferred from Bayesian analysis of a) 5 nuclear genes in *BEAST and b) 2,733 ultraconserved element loci in SNAPP. For each plot, the MCC phylogram (single bold bifurcating tree) is plotted over 5,000 trees drawn from the posterior distribution of each analysis (underlying shaded trees). Outgroups (differing for each study) were trimmed for clarity. Shading on nodes reflects ranges of Bayesian posterior probability values as described in the legend. Representatives of the brunneus and endemicus lineages were pooled here as “U. brunneus” given their close genetic relationship.

Fig. 3.

Cranial shape variation in 6 nuclear DNA lineages of small-eared Urocitellus based on 24 two-dimensional landmarks. a) Plots of group-wide variation from canonical axes 1 and 2 (top), and 1 and 3 (bottom). b) Heatmap of classification accuracies among all pairwise combinations of the 6 genetic lineages. Percent accurate classifications for each species are specified with numbers on the diagonal. b = brunneus, c = canus, w = washingtoni, t = townsendii, m (North) = northern mollis, m (South) = southern mollis. The cladogram at the bottom is the tree in Fig. 2b. Representatives of the brunneus and endemicus lineages were pooled here due to low sample sizes.

Fig. 4.

Principal component analysis of cranial morphology among U. mollis sensu lato subspecies based on a) 14 traditional linear measurements and b) 24 two-dimensional geometric morphometric (GMM) landmarks. The GMM data are representative of the ventral cranium only.

Fig. 5.

Ridgeline plots showing distributions of 3 external body measurements in lineages of small-eared Urocitellus. Representatives of the brunneus and endemicus lineages were pooled here due to low sample sizes. U. mollis artemesiae and U. m. idahoensis represent a single clade (e.g., Fig. 2) but are plotted separately here.