Slender salamanders (genusBatrachoseps) reveal Southern California to be a center for the diversification, persistence, and introduction of salamander lineages
Authors: Jockusch Elizabeth L. , Hansen Robert W. , Fisher Robert N. , Wake David B. 
Published: August 2020

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 majorandB. nigriventris, are relatively widely distributed in southern California, and estimated to have persisted there across millions of years. Recently several extralimital populations ofBatrachosepswere 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 ofB. major.

Methods

We sequenced the mitochondrial genecytochrome bfrom a geographically comprehensive sampling of the mitochondrial lineages ofB. majorandB. nigriventristhat 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 bothBatrachosepsspecies and four other salamander species with which they co-occur in southern California.

Results

The northern lineage ofB. majorharbors 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 nigriventrisalso has multiple deeply differentiated clades within the region. Comparative analyses highlight the smaller spatial scales over which mitochondrial divergence accumulates inBatrachosepsrelative to most other salamander species in southern California. The extralimital populations ofBatrachosepsfrom the San Joaquin Valley are assigned toB. majorand are shown to result from at least two independent introductions from different source populations. We also suggest thatB. majoron 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 inBatrachosepslikely also contribute to its propensity for introductions, and we anticipate that additional introduced populations will be discovered.