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 flagship species the 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 and those able to forego metamorphosis and retain a larval, aquatic lifestyle (i.e., paedomorphosis). Such disparate life history strategies are assumed to cause populations to become reproductively isolated, but the degree to which they have actually shaped population- and species-level boundaries is poorly understood. Using a large multi-locus dataset from hundreds of samples across North America, we identified genetic clusters with clear signs of admixture across the geographic range of the tiger salamander complex. Population clusters often contain a mixture of paedomorphic and metamorphic taxa, and we conclude that geography has played a large role in driving lineage divergence relative to obligate paedomorphosis in this system. This conclusion is bolstered by model-based analyses demonstrating gene flow between metamorphic and paedomorphic populations. Even the axolotl, a paedomorphic species with an isolated native range, apparently has a history of gene flow with its neighboring 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. The axolotl is currently used as the vertebrate model system in regenerative biology, and our findings chart a course for more informed use of these and other tiger salamander species in experimental and field research, including conservation priorities.

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

“…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.…”

“…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)…”

“…Ambystoma subsalsum was described by Taylor (1943) based on a metamorphosized type specimens in the vicinity of Lake Archichicha, but Brandon et al (1982) assigned metamorphosized individuals near Lake Archichicha to A. velasci and assigned aquatic individuals to the species A. taylori . 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).…”

“…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.…”

“…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).…”