Alex Pyron’s research while affiliated with George Washington University and other places

Numerous mechanisms drive ecological speciation, including isolation by adaptation, barrier, distance, environment, hierarchy, and resistance. These promote genetic and phenotypic differentiation of local populations, formation of phylogeographic lineages, and ultimately, completed speciation via reinforcement. In contrast, it is possible that similar mechanisms might lead to lineage cohesion through stabilizing rather than diversifying ecomorphological selection and the long-term persistence of population structure within species. Processes that drive the formation and maintenance of geographic genetic diversity while facilitating high rates of migration and limiting phenotypic divergence may thereby result in population structure that is not accompanied by divergence towards reproductive isolation. We suggest that this framework can be applied more broadly to address the classic dilemma of “structure versus speciation” 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 4 phylogenomic lineages with broad admixture across geographic hybrid zones, which could potentially represent distinct species. However, while limited dispersal promotes substantial isolation by distance, extreme microhabitat specificity appears to yield stabilizing selection on ecologically mediated phenotypes. As a result, climatic cycles promote recurrent contact between lineages that are not adaptively differentiated and therefore experience repeated bouts of high migration and introgression through time. This leads to a unified, single species with deeply divergent phylogeographic lineages that nonetheless do not appear to represent incipient species.

Species that went extinct prior to the genomic era are typically out-of-reach for modern phylogenetic studies. We refer to these as “Alexandrian” extinctions, after the lost library of the ancient world. This is particularly limiting for conservation studies, as genetic data for such taxa may be key to understand extinction threats and risks, the causes of declines, and inform management of related, extant populations. Fortunately, continual advances in biochemistry and DNA sequencing offer increasing ability to recover DNA from historical museum specimens, including fluid-preserved natural history collections. Here, we report on success in recovering nuclear and mitochondrial data from the apparently-extinct subspecies Desmognathus fuscus carri (Neill 1951), a plethodontid salamander from spring runs in central Florida. The two specimens are 50 years old and were likely preserved in unbuffered formalin, but application of a recently derived extraction procedure yielded usable DNA and partially successful Anchored Hybrid Enrichment sequencing. These data suggest that the populations of D. f. carri from peninsular Florida are conspecific with the D. auriculatus A lineage as suggested by previous authors, but likely represented an ecogeographically distinct genetic segment that has now been lost. Genetic data from this Alexandrian extinction thus confirm the geographic extent of population declines and extirpations as well as their ecological context, suggesting a possibly disproportionate loss from sandy-bottom clearwater streams compared to blackwater swamps. Success of these methods bodes well for large-scale application to fluid-preserved natural history specimens from relevant historical populations, but the possibility of significant DNA damage and related sequencing errors in additional hurdle to overcome.