Post-Pleistocene differentiation in a Central Interior Highlands endemic salamander

Abstract

Aim: For many endemic species with limited dispersal capacities, the relationship between landscape changes and species distributions is still unclear. We characterized the population structure of the endemic ringed salamander (Ambystoma annulatum) across its distribution in the Central Interior Highlands (CIH) of North America, an area of high species endemism, to infer the ecological and evolutionary history of the species.

Methods: We sampled 498 individuals across the species distribution and characterized the population genetic structure using nuclear microsatellite and mitochondrial DNA (mtDNA) markers.

Results: Ambystoma annulatum exist in two strongly supported nuclear genetic clusters across the CIH that correspond to a northern cluster that includes the Missouri Ozark populations and a southern cluster that includes the Arkansas and Oklahoma Ozarks and the Ouachita Mountains. Our demographic models estimated that these populations diverged approximately 2,700 years ago. Pairwise estimates of genetic differentiation at microsatellite and mtDNA markers indicated limited contemporary gene flow and suggest that genetic differentiation was primarily influenced by changes in the post-Pleistocene landscape of the CIH.

Main conclusions: Both the geologic history and post-European settlement history of the CIH have influenced the population genetic structure of A. annulatum. The low mtDNA diversity suggests a retraction into and expansion out of refugial areas in the south-central Ozarks, during temperature fluctuations of the Pleistocene and Holocene epochs. Similarly, the estimated divergence time for the two nuclear clusters corresponds to changes in the post-Pleistocene landscape. More recently, decreased A. annulatum gene flow may be a result of increased habitat fragmentation and alteration post-European settlement.

Keywords: Ambystoma annulatum; Ambystomatidae; Caudata; Ouachita Mountains; Ozark Highlands; Urodela; amphibians; biogeography.

Figure 1

Known occurrence locations and sampling sites for Ambystoma annulatum within the International Union for the Conservation of Nature (IUCN) distribution overlaid on a simplified 2011 Land Use, Land Cover layer. “Forest” habitats include broadleaf, mixed, and coniferous forests, and other shrub/scrub land use classes. “Herbaceous” habitats include agricultural fields, prairie, and other herbaceous habitats. Sampling sites are indicated by the large circles

Figure 2

Spatial distribution of genetic cluster assignments for Ambystoma annulatum computed in the program structure overlaid on a simplified 2011 Land Use, Land Cover layer. Admixture coefficients for individual A. annulatum from (a) all sites (as identified in Table 1) and (b) from each of the two supported genetic clusters identified in our full analysis. Spatial arrangement of genetic structure for A. annulatum across its distribution (c). Ellipses color corresponds to the admixture assignment scores from the full analysis (a) and pie colors correspond to admixture assignment scores from the two independent analyses for hierarchical substructure of individuals within each of the two presumed genetic clusters (b)

Figure 3

Spatial arrangement of mtDNA haplotypes by sampling location for Ambystoma annulatum. For each color, the proportion of the pie corresponds to the frequency of the haplotype in that population as outlined in Table 3. Colors correspond to the haplotypes represented in the median‐joining haplotype network, shown in the callout box. Each dash indicates a 1 bp difference between the connected haplotypes. White boundary corresponds to the International Union for the Conservation of Nature (IUCN) species distribution