Closing the ring: historical biogeography of the salamander ring species Ensatina eschscholtzii

Abstract

Aim The salamander Ensatina eschscholtzii Gray is a classic example of a ring species, or a species that has expanded around a central barrier to form a secondary contact characterized by species-level divergence. In the original formulation of the ring species scenario, an explicit biogeographical model was proposed to account for the occurrence of intraspecific sympatry between two subspecies in southern California (the 'southern closure' model). Here we develop an alternative ring species model that is informed by the geomorphological development of the California Coast Ranges, and which situates the point of ring closure in the Monterey Bay region of central coastal California (the 'Monterey closure' model). Our study has two aims. The first is to use phylogenetic methods to evaluate the two competing biogeographical models. The second is to describe patterns of phylogeographical diversity throughout the range of the Ensatina complex, and to compare these patterns with previously published molecular systematic data.Location Western North America, with a focus on the state of California, USA.Methods We obtained mitochondrial DNA sequence data from 385 individuals from 224 populations. A phylogeny was inferred using Bayesian techniques, and the geographical distributions of haplotypes and clades were mapped. The two biogeographical ring species models were tested against our Bayesian topology, including the associated Bayesian 95% credible set of trees.Results High levels of phylogeographical diversity were revealed, especially in central coastal and northern California. Our Bayesian topology contradicts the Monterey closure model; however, 0.08% of the trees in our Bayesian 95% credible set are consistent with this model. In contrast, the classic ring species biogeographical model (the southern closure model) is consistent with our Bayesian topology, as were 99.92% of the trees in our 95% credible set.Main conclusions Our Bayesian phylogenetic analysis most strongly supports the classic ring species model, modified to accommodate an improved understanding of the complex geomorphological evolution of the California Coast Ranges. In addition, high levels of phylogeographical diversity in central and northern California were identified, which is consistent with the striking levels of allozymic differentiation reported previously from those regions.

Evolution and stability of ring species

“…Despite some taxonomic controversy, the E. eschscholtzii complex is still one of the few well-documented ring species (reviewed in ref. 30), and it occurs in sympatry with other salamander genera (27).…”

“…Consistent with the importance of neutral divergence in the formation of ring species, for the salamander Ensatina eschscholtzii, a second well-documented ring species (reviewed in ref. 30), divergence in neutral nuclear markers is a better predictor of reproductive isolation than ecological divergence (31).…”

Wherefore and Whither the Ring Species?

“…Home ranges are small (on the order of a few square meters), dispersal is limited, and territories are defended (Stebbins, 1954;Staub et al, 1995;Wiltenmuth, 1996;Wiltenmuth and Nishikawa, 1998). Territoriality and limited vagility have led to the build-up of high levels of population genetic structure across the range of Ensatina (Kuchta et al, 2009a(Kuchta et al, , 2009bPereira and Wake, 2009). The hypothesis that Ensatina is a ring species was first advanced by Stebbins (1949) as part of a pioneering analysis that was part taxonomic revision, part evolutionary hypothesis.…”

“…The ranges of the seven subspecies are illustrated with different colors, along with representative photographs. Illustrating variation in Ensatina is challenging because phenotypic variation is often gradual (Stebbins, 1949) and broader than the genetic transitions (Kuchta et al, 2009a;Pereira and Wake, 2009). On this map, gradations between subspecies illustrate the borders identified by genetic markers.…”

“…A second phylogeographic study by Kuchta et al (2009a) followed Moritz et al (1992), but with denser geographic sampling. Their goal was to revisit the biogeographic scenario of Stebbins (1949), with a focus on the geomorphological evolution of the California Coast Range system.…”