Thriving in the Cold: Glacial Expansion and Post-Glacial Contraction of a Temperate Terrestrial Salamander (Plethodon serratus)

Abstract

The dynamic geologic history of the southeastern United States has played a major role in shaping the geographic distributions of amphibians in the region. In the phylogeographic literature, the predominant pattern of distribution shifts through time of temperate species is one of contraction during glacial maxima and persistence in refugia. However, the diverse biology and ecology of amphibian species suggest that a "one-size-fits-all" model may be inappropriate. Nearly 10% of amphibian species in the region have a current distribution comprised of multiple disjunct, restricted areas that resemble the shape of Pleistocene refugia identified for other temperate taxa in the literature. Here, we apply genetics and spatially explicit climate analyses to test the hypothesis that the disjunct regions of these species ranges are climatic refugia for species that were more broadly distributed during glacial maxima. We use the salamander Plethodon serratus as a model, as its range consists of four disjunct regions in the Southeast. Phylogenetic results show that P. serratus is comprised of multiple genetic lineages, and the four regions are not reciprocally monophyletic. The Appalachian salamanders form a clade sister to all other P. serratus. Niche and paleodistribution modeling results suggest that P. serratus expanded from the Appalachians during the cooler Last Glacial Maximum and has since been restricted to its current disjunct distribution by a warming climate. These data reject the universal applicability of the glacial contraction model to temperate taxa and reiterate the importance of considering the natural history of individual species.

Fig 1. Map of collection localities.

Numbers correspond to map code in Table 1. Inset: Ouachita region. OK = Oklahoma; AR = Arkansas. Photograph: P. serratus, LSUMZ 98343; photo credit: C.C.A.

Fig 2. Maximum-likelihood phylogeny of mitochondrial cytb.

Nodal support: grey dots: Bayesian PP > 0.9; black dots: ML bootstrap > 0.75 and Bayesian PP > 0.9. Shapes on the phylogeny correspond to map. Inset: Ouachita region.

Fig 3. Structure clusters (K = 5) for the nuclear data set.

Populations with individuals with the 9 bp deletion in the c3 locus are indicated by asterisks on the Ouachita inset. Colors and labels correspond to Fig 4.

Fig 4. Species tree from *BEAST.

Colors correspond to Structure bar plots in Fig 3. Nodal support: Bayesian PP.

Fig 5. Ecological niche models (second row) and paleodistribution models (mid-Holocene, LGM, LIG).

Columns: the four regions of the P. serratus range. Red line in the Appalachians denotes the French Broad River. For LGM models, note the expanded coastlines due to lower sea levels. For Ozark LIG model, note the area of suitability covers the entire depicted region.