Genetic Variation and Metapopulation Structure Inform Recovery Goals in a Threatened Species

Abstract

Background: Monitoring genetic parameters is important for setting effective conservation and management strategies, particularly for small, fragmented, and isolated populations. Small, isolated populations face increased rates of genetic drift and inbreeding, which increase extinction risk especially when gene flow is limited.

Methods: Here, we applied a Genotyping-in-Thousands by sequencing (GT-seq) panel to inform recovery action for the federally threatened northern Idaho ground squirrel (Urocitellus brunneus). We evaluated genetic diversity, structure, connectivity, and effective population size to address species recovery goals.

Results: We delineated three types of conservation units: (1) three evolutionarily significant units that represent long-term population structure and variation, (2) nine management units that reflect current demographic connectivity and restrictions to gene flow, and (3) three adaptive units that capture adaptive differentiation across the species range. Effective population sizes per management unit were small overall (mean 38.16, range 2.3-220.9), indicating that recovery goals of 10 subpopulations with N_e > 500 have not been reached.

Conclusions: Our results support the maintenance of connectivity within evolutionarily significant units through the restoration of dispersal corridors. Next steps could include further sampling of some subpopulations with low sample sizes, unsampled subpopulations, and subpopulations that are geographically isolated. Genotyping future samples with the same GT-seq panel would help to detect dispersal, assess effective population size, monitor the effects of inbreeding, and evaluate adaptive differentiation to monitor the effects of management action and environmental change.

Keywords: GT-seq; Urocitellus; conservation units; effective population size; ground squirrels.

Figure 1

Location of sampling sites within the NIDGS range in central Idaho, USA, including the years each site was sampled. (a) Outline of Idaho with range of NIDGS in dark gray. (b) Detail of NIDGS range with sampling sites denoted by color (which correspond to PCAs and population graphs in subsequent figures); full site names are in Table 1. Shape represents collection year: diamond = 2016, triangle = 2020, circle = 2016 and 2020, square = Round Valley in 2022. NIDGS range obtained from https://ecos.fws.gov/ecp/species/2982 (accessed on 6 June 2024).

Figure 2

Outputs from PCA and STRUCTURE used to delineate three ESUs. (a) PCA with all SNPs; circles represent samples from 2016, and triangles represent samples from 2020. Colors correspond to site labels in Figure 1. (b) Ancestry values from STRUCTURE are given as pie charts plotted on the NIDGS range. Each color represents a distinct genetic cluster.

Figure 3

Outputs from pairwise F_ST, PCA, and STRUCTURE used to delineate nine MUs for the NIDGS. (a) Pairwise F_ST heatmap with neutral SNPs for 2016 samples. Blue represents F_ST values of 0 and red represents F_ST values of 0.2. (b) Pairwise F_ST heatmap with neutral SNPs for 2020 samples. Blue represents F_ST values of 0 and red represents F_ST values of 0.3. (c) PCA with neutral SNPs, circles represent samples from 2016, and triangles represent samples from 2020. Colors correspond to site labels in Figure 1. (d) Ancestry values from STRUCTURE with neutral SNPs are given as pie charts plotted on the NIDGS range. Each color represents a distinct genetic cluster.

Figure 4

Saturated spatial population graph illustrating the gene flow between NIDGS sites for (a) 2016 and (b) 2020. Edges shown are flow predictions (flow = 1 − Nei’s D): dotted = 0.85–0.90; dashed = 0.90–0.95; solid = 0.95–1.0. The sizes of the nodes are scaled to measure degree (total number of edges connected to a particular node), and the color represents sites and is the same as Figure 1 and all the PCAs.

Figure 5

Outputs from PCA and STRUCTURE used to delineate three AUs for the NIDGS. (a) PCA with putatively adaptive SNPs, circles represent samples from 2016, and triangles represent samples from 2020. Colors correspond to site labels in Figure 1. (b) Ancestry values from STRUCTURE with adaptive SNPs are given as pie charts plotted on the NIDGS range. Each color represents a distinct genetic cluster.