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ABSTRACT AimWe tested whether co‐distributed phrynosomatid lizards in the Baja California Peninsula (BCP) share synchronous phylogeographic discontinuities, as predicted by the “peninsular archipelago” hypothesis, and examined the diversification ofCallisaurus draconoidesthroughout its range. LocationThe BCP and the Great Basin, Mojave and Sonoran Deserts of southwestern North America. TaxaFive co‐distributed species complexes representing four genera within Phrynosomatidae:Callisaurus,Petrosaurus,UrosaurusandSceloporus. MethodsDouble‐digest restriction‐associated‐DNA (ddRAD) sequencing was used to collect genome‐wide sequence data for 309 lizards. We used phylogenetic analyses of concatenated loci and population admixture analysis of unlinked SNPs to identify lineages. To infer a species tree, we collected target sequence capture (TSC) data. Migration between adjacent peninsular lineages was estimated using the multispecies coalescent with migration (MSC‐M) in BPP. A full‐likelihood Bayesian comparative phylogeographic approach (ecoevolity) was used to test the simultaneous divergence hypothesis for the Isthmus of La Paz and Vizcaíno Desert. ResultsWe identified 24 potential lineages within the five co‐distributed complexes. Contact zones between lineages were observed at the Isthmus of La Paz in four of the five complexes, and in all five within the Vizcaíno Desert. The time‐calibrated species tree indicates that within each complex, divergences at the Isthmus of La Paz predate those across the Vizcaíno Desert. We found strong support for at least three independent divergence events at the Isthmus of La Paz and the Vizcaíno Desert, thereby rejecting the simultaneous divergence hypothesis. Inferred migration rates between adjacent peninsular populations were generally low (M << 1) to absent. Zebra‐tailed lizards (Callisaurus), in which the earliest diverging lineages are endemic to the southern BCP, exhibit a clear pattern of Pleistocene range expansion from the BCP into the deserts of the western United States and mainland Mexico. The most deeply nested populations inCallisaurusoccur at the northern, eastern and southeastern range limits in temperate, subtropical and tropical biomes, respectively. Main ConclusionsThese results support the BCP's tectonic isolation as a driver of peninsular endemism and a contributing factor to lineage diversification more broadly in the region. Taxonomic adjustments, including resurrectingUrosaurus microscutatus, are proposed to better reflect evolutionary history in taxonomy. 

Abstract Parallel evolution of the same reproductive isolation barrier within a taxon is an indicator of ecology’s role in speciation (i.e., parallel speciation), yet spatiotemporal variability in the efficacy of the barrier can present challenges to retracing how it evolved. Here, we revisit the evidence for a candidate example of parallel speciation in a clade of scincid lizards (the Plestiodon skiltonianus complex) using genomic data, with emphasis on determining whether hybridization may have confounded the phylogenetic signals of parallelism for this group. Our results show a striking case of genealogical discordance, in which mitochondrial loci support multiple origins of a derived large-bodied morphotype (Plestiodon gilberti) within a small-bodied ancestor (Plestiodon skiltonianus), whereas nuclear loci indicate a single origin. We attribute the discordance to separate, temporally-spaced hybridization events that led to asymmetric capture of P. skiltonianus mitochondria in different regional lineages of P. gilberti. Nuclear introgression showed a similar directional bias but was less pervasive. We demonstrate how a mechanical reproductive barrier previously identified for this group explains the asymmetry of mitochondrial introgression, given that hybrid matings are most likely when the male is P. gilberti and the female is P. skiltonianus. We then use permutation tests of morphological data to provide evidence that the mechanical barrier is less stringent in areas where hybridization is inferred to have occurred. Our results demonstrate how biased hybridization can dictate which genetic variants are transmitted between species and emphasize the importance of accounting for introgression and deep coalescence in identifying phyletic signatures of parallel speciation. 

ABSTRACT Coalescent modelling of hybrid zones can provide novel insights into the historical demography of populations, including divergence times, population sizes, introgression proportions, migration rates and the timing of hybrid zone formation. We used coalescent analysis to determine whether the hybrid zone between phylogeographic lineages of the Plateau Fence Lizard (Sceloporus tristichus) in Arizona formed recently due to human‐induced landscape changes, or if it originated during Pleistocene climatic shifts. Given the presence of mitochondrial DNA from another species in the hybrid zone (Southwestern Fence Lizard,S. cowlesi), we tested for the presence ofS. cowlesinuclear DNA in the hybrid zone as well as reassessed the species boundary betweenS. tristichusandS. cowlesi. No evidence ofS. cowlesinuclear DNA is found in the hybrid zone, and the paraphyly of both species raises concerns about their taxonomic validity. Introgression analysis placed the divergence time between the parental hybrid zone populations at approximately 140 kya and their secondary contact and hybridization at approximately 11 kya at the end of the Pleistocene. Introgression proportions estimated for hybrid populations are correlated with their geographic distance from parental populations. The multispecies coalescent with migration provided significant support for unidirectional migration moving from south to north, which is consistent with spatial cline analyses that suggest a slow but steady northward shift of the centre of the hybrid zone over the last two decades. When analysing hybrid populations sampled along a linear transect, coalescent methods can provide novel insights into hybrid zone dynamics. 

Abstract Phrynosoma mcallii(flat‐tailed horned lizards) is a species of conservation concern in the Colorado Desert of the United States and Mexico. We analysed ddRADseq data from 45 lizards to estimate population structure, infer phylogeny, identify migration barriers, map genetic diversity hotspots, and model demography. We identified the Colorado River as the main geographic feature contributing to population structure, with the populations west of this barrier further subdivided by the Salton Sea. Phylogenetic analysis confirms that northwestern populations are nested within southeastern populations. The best‐fit demographic model indicates Pleistocene divergence across the Colorado River, with significant bidirectional gene flow, and a severe Holocene population bottleneck. These patterns suggest that management strategies should focus on maintaining genetic diversity on both sides of the Colorado River and the Salton Sea. We recommend additional lands in the United States and Mexico that should be considered for similar conservation goals as those in the Rangewide Management Strategy. We also recommend periodic rangewide genomic sampling to monitor ongoing attrition of diversity, hybridization, and changing structure due to habitat fragmentation, climate change, and other long‐term impacts. 

Abstract 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. 

Abstract The opposing forces of gene flow and isolation are two major processes shaping genetic diversity. Understanding how these vary across space and time is necessary to identify the environmental features that promote diversification. The detection of considerable geographic structure in taxa from the arid Nearctic has prompted research into the drivers of isolation in the region. Several geographic features have been proposed as barriers to gene flow, including the Colorado River, Western Continental Divide (WCD), and a hypothetical Mid-Peninsular Seaway in Baja California. However, recent studies suggest that the role of barriers in genetic differentiation may have been overestimated when compared to other mechanisms of divergence. In this study, we infer historical and spatial patterns of connectivity and isolation in Desert Spiny Lizards (Sceloporus magister) and Baja Spiny Lizards (Sceloporus zosteromus), which together form a species complex composed of parapatric lineages with wide distributions in arid western North America. Our analyses incorporate mitochondrial sequences, genomic-scale data, and past and present climatic data to evaluate the nature and strength of barriers to gene flow in the region. Our approach relies on estimates of migration under the multispecies coalescent to understand the history of lineage divergence in the face of gene flow. Results show that the S. magister complex is geographically structured, but we also detect instances of gene flow. The WCD is a strong barrier to gene flow, while the Colorado River is more permeable. Analyses yield conflicting results for the catalyst of differentiation of peninsular lineages in S. zosteromus. Our study shows how large-scale genomic data for thoroughly sampled species can shed new light on biogeography. Furthermore, our approach highlights the need for the combined analysis of multiple sources of evidence to adequately characterize the drivers of divergence. 

Abstract BackgroundHigh-quality genomic resources facilitate investigations into behavioral ecology, morphological and physiological adaptations, and the evolution of genomic architecture. Lizards in the genus Sceloporus have a long history as important ecological, evolutionary, and physiological models, making them a valuable target for the development of genomic resources. FindingsWe present a high-quality chromosome-level reference genome assembly, SceUnd1.0 (using 10X Genomics Chromium, HiC, and Pacific Biosciences data), and tissue/developmental stage transcriptomes for the eastern fence lizard, Sceloporus undulatus. We performed synteny analysis with other snake and lizard assemblies to identify broad patterns of chromosome evolution including the fusion of micro- and macrochromosomes. We also used this new assembly to provide improved reference-based genome assemblies for 34 additional Sceloporus species. Finally, we used RNAseq and whole-genome resequencing data to compare 3 assemblies, each representing an increased level of cost and effort: Supernova Assembly with data from 10X Genomics Chromium, HiRise Assembly that added data from HiC, and PBJelly Assembly that added data from Pacific Biosciences sequencing. We found that the Supernova Assembly contained the full genome and was a suitable reference for RNAseq and single-nucleotide polymorphism calling, but the chromosome-level scaffolds provided by the addition of HiC data allowed synteny and whole-genome association mapping analyses. The subsequent addition of PacBio data doubled the contig N50 but provided negligible gains in scaffold length. ConclusionsThese new genomic resources provide valuable tools for advanced molecular analysis of an organism that has become a model in physiology and evolutionary ecology. 

Abstract In the past two decades, genomic data have been widely used to detect historical gene flow between species in a variety of plants and animals. The Tamias quadrivittatus group of North America chipmunks, which originated through a series of rapid speciation events, are known to undergo massive amounts of mitochondrial introgression. Yet in a recent analysis of targeted nuclear loci from the group, no evidence for cross-species introgression was detected, indicating widespread cytonuclear discordance. The study used the heuristic method HYDE to detect gene flow, which may suffer from low power. Here we use the Bayesian method implemented in the program BPP to re-analyze these data. We develop a Bayesian test of introgression, calculating the Bayes factor via the Savage-Dickey density ratio using the Markov chain Monte Carlo (MCMC) sample under the model of introgression. We take a stepwise approach to constructing an introgression model by adding introgression events onto a well-supported binary species tree. The analysis detected robust evidence for multiple ancient introgression events affecting the nuclear genome, with introgression probabilities reaching 63%. We estimate population parameters and highlight the fact that species divergence times may be seriously underestimated if ancient cross-species gene flow is ignored in the analysis. We examine the assumptions and performance of HYDE and demonstrate that it lacks power if gene flow occurs between sister lineages or if the mode of gene flow does not match the assumed hybrid-speciation model with symmetrical population sizes. Our analyses highlight the power of likelihood-based inference of cross-species gene flow using genomic sequence data. [Bayesian test; BPP; chipmunks; introgression; MSci; multispecies coalescent; Savage-Dickey density ratio.] 

Abstract 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. 

Abstract Divergence is often ephemeral, and populations that diverge in response to regional topographic and climatic factors may not remain reproductively isolated when they come into secondary contact. We investigated the geographical structure and evolutionary history of population divergence withinSceloporus occidentalis(western fence lizard), a habitat generalist with a broad distribution that spans the major biogeographical regions of Western North America. We used double digest RAD sequencing to infer population structure, phylogeny and demography. Population genetic structure is hierarchical and geographically structured with evidence for gene flow between biogeographical regions. Consistent with the isolation–expansion model of divergence during Quaternary glacial–interglacial cycles, gene flow and secondary contact are supported as important processes explaining the demographic histories of populations. Although populations may have diverged as they spread northward in a ring‐like manner around the Sierra Nevada and southern Cascade Ranges, there is strong evidence for gene flow among populations at the northern terminus of the ring. We propose the concept of an “ephemeral ring species” and contrastS. occidentaliswith the classic North American ring species,Ensatina eschscholtzii. Contrary to expectations of lower genetic diversity at northern latitudes following post‐Quaternary‐glaciation expansion, the ephemeral nature of divergence inS. occidentalishas produced centres of high genetic diversity for different reasons in the south (long‐term stability) vs. the north (secondary contact).