Kinship and Breeding Site Philopatry Drive Fine-Scale Genetic Structure in Fragmented Populations of the Gopher Frog (Rana capito) in North Carolina
The Gopher Frog (Rana capito) is a threatened species native to the southeastern longleaf pine ecosystem. Although once much more widespread across the southeastern United States, they now occur in North Carolina at only a handful of disjunct sites in the Coastal Plain and Sandhills regions of the state. The long-term persistence of these populations is thus a concern, as is a loss of genetic variation over time. We used mitochondrial and microsatellite markers to better understand the spatial structure of genetic variation and levels of genetic variability across these remaining populations in order to inform conservation and management decisions. Eight unique mitochondrial haplotypes were found, but these were all genetically similar to one another. Levels of genetic diversity based on the microsatellite analyses were similar across populations, but inbreeding coefficients in two populations were significant, suggesting a potential vulnerability to inbreeding depression. All disjunct populations showed significant genetic differentiation, which was not related to geographic distance. Conversely, within populations, the genetic relatedness of individuals between ponds decreased as distance between ponds increased. This kinship pattern is likely driven by strong breeding philopatry (individuals returning to the same ponds across years) and indicates that conservation actions at the scale of <1 km would primarily affect kin groups of Gopher Frogs, whereas conservation actions at scales ≥1.5 km would be needed to capture more distantly related individuals. Management efforts should thus focus on local metapopulation dynamics by maintaining multiple breeding ponds at each location, and by enhancing connectivity between these breeding ponds.ABSTRACT
Map displaying the locations (circles) of known Gopher Frog (Rana capito) populations in North Carolina. These populations are located at Boiling Spring Lakes (BSL), Holly Shelter Game Lands (Holly Shelter), Military Ocean Terminal Sunny Point-Southport (Southport), Sandhills Game Lands (Sandhills), Croatan Game Lands (Croatan), Fort Bragg (Bragg), and Camp Lejeune (Lejeune). BSL is designated with a gray circle because only two individuals were analyzed (with mtDNA only) for this site and Bragg is designated with a white circle because no samples from this location were analyzed in this study (see Methods).
Maximum-likelihood phylogenetic tree of Gopher Frog ND2 haplotypes (blue). Included are the eight ND2 mtDNA haplotypes we observed in newly sequenced individuals of R. capito sampled from throughout North Carolina (bold) and eight ND2 reference haplotypes taken from Richter et al. (2014). Four ND2 sequences of the Crawfish Frog (R. aureolata; black) from Richter et al. (2014) were used as outgroup taxa in the phylogenetic analysis. All individuals of North Carolina R. capito that we sequenced belong to the Southeastern Coastal Clade, one of three lineages of R. capito originally identified by Richter et al. (2014). A full summary of all of the samples we examined and the haplotype group to which they were assigned is presented in Supplemental Data, Tables S1, S2.
Isolation by distance: regression of genetic distance (mean r) vs. geographic distance (km) for (a) population pairs (regional scale) and (b) pond pairs within a population (local scale).
Proportion of observed kinship comparisons for each population that were more or less than expected for each of four kinship categories (nearly identical: 0.375 < k < 0.57; full sibling: 0.1875 < k < 0.375; half sibling: 0.09375 < k < 0.1875; and quarter sibling: 0.047 < k < 0.09375). Zero refers to those individuals who are unrelated. Expected numbers of kinship comparisons for each category based on pairwise kinship coefficients that were calculated after randomly shuffling individuals among populations. * Significant differences at P < 0.05.
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