Slender salamanders (genus Batrachoseps) reveal Southern California to be a center for the diversification, persistence, and introduction of salamander lineages

Abstract

Background The southern California biodiversity hotspot has had a complex geological history, with both plate tectonic forces and sea level changes repeatedly reconfiguring the region, and likely driving both lineage splittings and extinctions. Here we investigate patterns of genetic divergence in two species of slender salamanders (Plethodontidae: Batrachoseps) in this region. The complex geological history in combination with several organismal traits led us to predict that these species harbor multiple ancient mitochondrial lineages endemic to southern California. These species belong to a clade characterized by fine-scale mitochondrial structure, which has been shown to track ancient splits. Both focal species, Batrachoseps major and B. nigriventris, are relatively widely distributed in southern California, and estimated to have persisted there across millions of years. Recently several extralimital populations of Batrachoseps were found in the San Joaquin Valley of California, a former desert area that has been extensively modified for agriculture. The origins of these populations are unknown, but based on morphology, they are hypothesized to result from human-mediated introductions of B. major. Methods We sequenced the mitochondrial gene cytochrome b from a geographically comprehensive sampling of the mitochondrial lineages of B. major and B. nigriventris that are endemic to southern California. We used phylogenetic analyses to characterize phylogeographic structure and identify mitochondrial contact zones. We also included the San Joaquin Valley samples to test whether they resulted from introductions. We used a bootstrap resampling approach to compare the strength of isolation-by-distance in both Batrachoseps species and four other salamander species with which they co-occur in southern California. Results The northern lineage of B. major harbors at least eight deeply differentiated, geographically cohesive mitochondrial subclades. We identify geographic contact between many of these mtDNA lineages and some biogeographic features that are concordant with lineage boundaries. Batrachoseps nigriventris also has multiple deeply differentiated clades within the region. Comparative analyses highlight the smaller spatial scales over which mitochondrial divergence accumulates in Batrachoseps relative to most other salamander species in southern California. The extralimital populations of Batrachoseps from the San Joaquin Valley are assigned to B. major and are shown to result from at least two independent introductions from different source populations. We also suggest that B. major on Catalina Island, where it is considered native, may be the result of an introduction. Some of the same traits that facilitate the build-up of deep phylogeographic structure in Batrachoseps likely also contribute to its propensity for introductions, and we anticipate that additional introduced populations will be discovered.