Geography is more important than life history in the recent diversification of the tiger salamander complex

Abstract

The North American tiger salamander species complex, including its best-known species, the Mexican axolotl, has long been a source of biological fascination. The complex exhibits a wide range of variation in developmental life history strategies, including populations and individuals that undergo metamorphosis; those able to forego metamorphosis and retain a larval, aquatic lifestyle (i.e., paedomorphosis); and those that do both. The evolution of a paedomorphic life history state is thought to lead to increased population genetic differentiation and ultimately reproductive isolation and speciation, but the degree to which it has shaped population- and species-level divergence is poorly understood. Using a large multilocus dataset from hundreds of samples across North America, we identified genetic clusters across the geographic range of the tiger salamander complex. These clusters often contain a mixture of paedomorphic and metamorphic taxa, indicating that geographic isolation has played a larger role in lineage divergence than paedomorphosis in this system. This conclusion is bolstered by geography-informed analyses indicating no effect of life history strategy on population genetic differentiation and by model-based population genetic analyses demonstrating gene flow between adjacent metamorphic and paedomorphic populations. This fine-scale genetic perspective on life history variation establishes a framework for understanding how plasticity, local adaptation, and gene flow contribute to lineage divergence. Many members of the tiger salamander complex are endangered, and the Mexican axolotl is an important model system in regenerative and biomedical research. Our results chart a course for more informed use of these taxa in experimental, ecological, and conservation research.

Morphometric analyses of the vertebrae of Ambystoma (Tschudi, 1838) and the implications for identification of fossil salamanders

“…Cladogram of species of Ambystoma based on relationships recovered by Williams et al (2013) and Everson et al (2021). Clades A though H correspond to those recovered by Williams et al (2013) the parapopohysis are widely divergent and robust (Boardman & Schubert, 2011).…”

“…Although we list specimens in our data set as A. taylori, the status of A. taylori as a distinct species requires additional study (Everson et al, 2021). Similarly, some specimens in our data set labeled as A. tigrinum are listed here as A. mavortium on the basis that these species were split after the specimens were collected and their locality data indicate collection within the modern range of A. mavortium (Everson et al, 2021). All other specimen identifications on museum labels were accepted as valid.…”

“…Although we tried to only include mature individuals in our data set, a fossil vertebra from a juvenile individual of a particular species may be classified as the wrong species if the juvenile morphology more closely resembles the adult morphology of another species. This problem extends to forms that are paedomorphic, which is known in many species of Ambystoma (AmphibiaWeb, 2021) including several species in the tiger salamander species complex (Everson et al, 2021). In the case of Ambystoma, juveniles generally have much smaller vertebrae that are less well-ossified compared with adults of the same species.…”

“…Difficulty in distinguishing species within the tiger salamander species complex based on vertebral morphology is unsurprising given the non-trivial nature of distinguishing them genetically (Everson et al, 2021;Shaffer & McKnight, 1996). However, even fossil identifi- (Tipton et al, 2012;Toomey, 1993).…”

“…Additionally, in some cases, morphological features were given to identify species of Ambystoma that have since been split into multiple species. Ambystoma tigrinum, for example, was previously recognized as a wide-ranging species across much of the U.S. but has since been split into multiple species (Everson et al, 2021;Shaffer & McKnight, 1996). Therefore, when referencing A. tigrinum we specify whether it signifies A. tigrinum + species that are now recognized as distinct (sensu lato) or A. tigrinum as it is currently recognized (sensu stricto).…”