Discerning structure versus speciation in phylogeographic analysis of Seepage Salamanders (Desmognathus aeneus) using demography, environment, geography, and phenotype

Numerous mechanisms can drive speciation, including isolation by adaptation, distance, and environment. These forces can promote genetic and phenotypic differentiation of local populations, the formation of phylogeographic lineages, and ultimately, completed speciation. However, conceptually similar mechanisms may also result in stabilizing rather than diversifying selection, leading to lineage integration and the long-term persistence of population structure within genetically cohesive species. Processes that drive the formation and maintenance of geographic genetic diversity while facilitating high rates of migration and limiting phenotypic differentiation may thereby result in population genetic structure that is not accompanied by reproductive isolation. We suggest that this framework can be applied more broadly to address the classic dilemma of structure versus species when evaluating phylogeographic diversity, unifying population genetics, species delimitation, and the underlying study of speciation. We demonstrate one such instance in the Seepage Salamander (Desmognathus aeneus) from the southeastern United States. Recent studies estimated up to 6.3% mitochondrial divergence and four phylogenomic lineages with broad admixture across geographic hybrid zones, which could potentially represent distinct species supported by our species-delimitation analyses. However, while limited dispersal promotes substantial isolation by distance, microhabitat specificity appears to yield stabilizing selection on a single, uniform, ecologically mediated phenotype. As a result, climatic cycles promote recurrent contact between lineages and repeated instances of high migration through time. Subsequent hybridization is apparently not counteracted by adaptive differentiation limiting introgression, leaving a single unified species with deeply divergent phylogeographic lineages that nonetheless do not appear to represent incipient species.

Automated summary

Mechanisms and processes can drive speciation and differentiation, as well as stabilize population structures. Genetic and phenotypic differences among individuals can change with environmental changes. Processes that maintain geographic genetic diversity while facilitating high rates of migration and limiting phenotypic differentiation often do not result in reproductive isolation, but rather population genetic structures. This framework can be used to unify the study of population genetics, species delimitation, and speciation.