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Understanding the processes that shape genetic diversity by either promoting or preventing population divergence can help identify geographic areas that either facilitate or limit gene flow. Furthermore, broadly distributed species allow us to understand how biogeographic and ecogeographic transitions affect gene flow. We investigated these processes using genomic data in the Northern Alligator Lizard (Elgaria coerulea), which is widely distributed in Western North America across diverse ecoregions (California Floristic Province and Pacific Northwest) and mountain ranges (Sierra Nevada, Coastal Ranges, and Cascades). We collected single-nucleotide polymorphism data from 120 samples of E. coerulea. Biogeographic analyses of squamate reptiles with similar distributions have identified several shared diversification patterns that provide testable predictions for E. coerulea, including deep genetic divisions in the Sierra Nevada, demographic stability of southern populations, and recent post-Pleistocene expansion into the Pacific Northwest. We use genomic data to test these predictions by estimating the structure, connectivity, and phylogenetic history of populations. At least 10 distinct populations are supported, with mixed-ancestry individuals situated at most population boundaries. A species tree analysis provides strong support for the early divergence of populations in the Sierra Nevada Mountains and recent diversification into the Pacific Northwest. Admixture and migration analyses detect gene flow among populations in the Lower Cascades and Northern California, and a spatial analysis of gene flow identified significant barriers to gene flow across both the Sierra Nevada and Coast Ranges. The distribution of genetic diversity in E. coerulea is uneven, patchy, and interconnected at population boundaries. The biogeographic patterns seen in E. coerulea are consistent with predictions from co-distributed species.

 

Population dynamics within species at the edge of their distributional range, including the formation of genetic structure during range expansion, are difficult to study when they have had limited time to evolve. Western Fence Lizards (Sceloporus occidentalis) have a patchy distribution at the northern edge of their range around the Puget Sound, Washington, where they almost exclusively occur on imperiled coastal habitats. The entire region was covered by Pleistocene glaciation as recently as 16,000 years ago, suggesting that populations must have colonized these habitats relatively recently. We tested for population differentiation across this landscape using genome-wide SNPs and morphological data. A time-calibrated species tree supports the hypothesis of a post-glacial establishment and subsequent population expansion into the region. Despite a strong signal for fine-scale population genetic structure across the Puget Sound with as many as 8–10 distinct subpopulations supported by the SNP data, there is minimal evidence for morphological differentiation at this same spatiotemporal scale. Historical demographic analyses suggest that populations expanded and diverged across the region as the Cordilleran Ice Sheet receded. Population isolation, lack of dispersal corridors, and strict habitat requirements are the key drivers of population divergence in this system. These same factors may prove detrimental to the future persistence of populations as they cope with increasing shoreline development associated with urbanization.

 

Phylogenomic investigations of biodiversity facilitate the detection of fine-scale population genetic structure and the demographic histories of species and populations. However, determining whether or not the genetic divergence measured among populations reflects species-level differentiation remains a central challenge in species delimitation. One potential solution is to compare genetic divergence between putative new species with other closely related species, sometimes referred to as a reference-based taxonomy. To be described as a new species, a population should be at least as divergent as other species. Here, we develop a reference-based taxonomy for Horned Lizards ( Phrynosoma ; 17 species) using phylogenomic data (ddRADseq data) to provide a framework for delimiting species in the Greater Short-horned Lizard species complex ( P. hernandesi ). Previous species delimitation studies of this species complex have produced conflicting results, with morphological data suggesting that P. hernandesi consists of five species, whereas mitochondrial DNA support anywhere from 1 to 10 + species. To help address this conflict, we first estimated a time-calibrated species tree for P. hernandesi and close relatives using SNP data. These results support the paraphyly of P. hernandesi; we recommend the recognition of two species to promote a taxonomy that is consistent with species monophyly. There is strong evidence for three populations within P. hernandesi , and demographic modeling and admixture analyses suggest that these populations are not reproductively isolated, which is consistent with previous morphological analyses that suggest hybridization could be common. Finally, we characterize the population-species boundary by quantifying levels of genetic divergence for all 18 Phrynosoma species. Genetic divergence measures for western and southern populations of P. hernandesi failed to exceed those of other Phrynosoma species, but the relatively small population size estimated for the northern population causes it to appear as a relatively divergent species. These comparisons underscore the difficulties associated with putting a reference-based approach to species delimitation into practice. Nevertheless, the reference-based approach offers a promising framework for the consistent assessment of biodiversity within clades of organisms with similar life histories and ecological traits.