Nest-Site Fidelity and Sex-Biased Dispersal Affect Spatial Genetic Structure of Eastern Box Turtles (Terrapene carolina carolina) at Their Northern Range Edge
Dispersal and nesting philopatry are two processes that affect the connectivity, evolution, and long-term viability of populations, and thus have important conservation implications for threatened and endangered species. Here we investigate dispersal, relatedness, and the fine-scale spatial genetic structure of Eastern Box Turtles (Terrapene carolina carolina) at the northern extreme of their geographic range in northwestern Michigan. We analyzed georeferenced microsatellite genotypes (n = 165) using global, sex-specific, and two-dimensional local spatial autocorrelation (2D LSA), as well as spatial principal components analysis (sPCA). Genetic diversity was low relative to Eastern Box Turtle populations in the middle of the range. We found dispersal was male-biased, as only females showed significant positive spatial genetic autocorrelation at distances less than 2 km. 2D LSA showed local genetic “hotspots” of related turtles that tended to correspond with known nesting areas. We found evidence for global genetic structure using sPCA, which we attribute to genetic clustering rather than clinal variation. Our results suggest that restricted female dispersal and fidelity to limited open-canopy nest sites result in fine-scale spatial genetic structuring in this population. We stress the importance of maintaining high quality nesting habitat and habitat corridors for transient males, which appear to be critical for functional connectivity of Eastern Box Turtles.

Scatterplot showing the matrix of pairwise genetic distances and matrix of pairwise geographic distances for box turtles sampled along the river corridor. Warmer colors within the kernel density indicate higher densities of points. The line (slope = 1.074727e–05; R2 = 0.002992) shows the correlation trend.

Spatial genetic autocorrelograms of genetic correlation coefficients (r) as a function of distance for Eastern Box Turtles in northwestern Michigan. Plots represent (A) all individuals (n = 165), (B) females only (n = 104), and (C) males only (n = 51). Dashed lines are permuted 95% confidence intervals across all data, and error bars are bootstrapped 95% confidence intervals within each distance class. Tables below graphs represent data for each distance class including the number of pairwise comparisons (n), the correlation coefficients (r), and the P-values (p) associated with bootstrap tests of significance for positive spatial genetic autocorrelation.

Bubble plot showing the results of two-dimensional local spatial autocorrelation analysis for all Eastern Box Turtles (n = 165) sampled in northwestern Michigan. Circles represent individuals and the size of the circle is proportional to the P-values from permutation testing, with large circles representing individuals that are significantly more related to their five nearest neighbors than expected (P < 0.05) based on a random distribution of genotypes. Figure shows the distribution of five genetic “hotspots” in relation to known nesting sites (NS) across the study area. Some distantly sampled individuals are omitted for figure clarity.

Analysis of global structure along the river corridor from the first principal component of the sPCA represented by (A) interpolation of lagged principal scores showing genetic clines and (B) colors indicating individual scores. Coordinates have been deliberately omitted to deter poachers.
Contributor Notes
Associate Editor: J. D. Litzgus.