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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 tomore »the future persistence of populations as they cope with increasing shoreline development associated with urbanization.

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Abstract The southwestern and central United States serve as an ideal region to test alternative hypotheses regarding biotic diversification. Genomic data can now be combined with sophisticated computational models to quantify the impacts of paleoclimate change, geographic features, and habitat heterogeneity on spatial patterns of genetic diversity. In this study, we combine thousands of genotyping-by-sequencing (GBS) loci with mtDNA sequences (ND1) from the Texas horned lizard (Phrynosoma cornutum) to quantify relative support for different catalysts of diversification. Phylogenetic and clustering analyses of the GBS data indicate support for at least three primary populations. The spatial distribution of populations appears concordant with habitat type, with desert populations in AZ and NM showing the largest genetic divergence from the remaining populations. The mtDNA data also support a divergent desert population, but other relationships differ and suggest mtDNA introgression. Genotype–environment association with bioclimatic variables supports divergence along precipitation gradients more than along temperature gradients. Demographic analyses support a complex history, with introgression and gene flow playing an important role during diversification. Bayesian multispecies coalescent analyses with introgression (MSci) analyses also suggest that gene flow occurred between populations. Paleo-species distribution models support two southern refugia that geographically correspond to contemporary lineages. We find thatmore »divergence times are underestimated and population sizes are overestimated when introgression occurred and is ignored in coalescent analyses, and furthermore, inference of ancient introgression events and demographic history is sensitive to inclusion of a single recently admixed sample. Our analyses cannot refute the riverine barrier or glacial refugia hypotheses. Results also suggest that populations are continuing to diverge along habitat gradients. Finally, the strong evidence of admixture, gene flow, and mtDNA introgression among populations suggests that P. cornutum should be considered a single widespread species under the General Lineage Species Concept.« less

Background High-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. Findings We 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 associationmore »mapping analyses. The subsequent addition of PacBio data doubled the contig N50 but provided negligible gains in scaffold length. Conclusions These new genomic resources provide valuable tools for advanced molecular analysis of an organism that has become a model in physiology and evolutionary ecology.« less

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.more »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.« less

Abstract Genome sequencing projects routinely generate haploid consensus sequences from diploid genomes, which are effectively chimeric sequences with the phase at heterozygous sites resolved at random. The impact of phasing errors on phylogenomic analyses under the multispecies coalescent (MSC) model is largely unknown. Here, we conduct a computer simulation to evaluate the performance of four phase-resolution strategies (the true phase resolution, the diploid analytical integration algorithm which averages over all phase resolutions, computational phase resolution using the program PHASE, and random resolution) on estimation of the species tree and evolutionary parameters in analysis of multilocus genomic data under the MSC model. We found that species tree estimation is robust to phasing errors when species divergences were much older than average coalescent times but may be affected by phasing errors when the species tree is shallow. Estimation of parameters under the MSC model with and without introgression is affected by phasing errors. In particular, random phase resolution causes serious overestimation of population sizes for modern species and biased estimation of cross-species introgression probability. In general, the impact of phasing errors is greater when the mutation rate is higher, the data include more samples per species, and the species tree is shallowermore »with recent divergences. Use of phased sequences inferred by the PHASE program produced small biases in parameter estimates. We analyze two real data sets, one of East Asian brown frogs and another of Rocky Mountains chipmunks, to demonstrate that heterozygote phase-resolution strategies have similar impacts on practical data analyses. We suggest that genome sequencing projects should produce unphased diploid genotype sequences if fully phased data are too challenging to generate, and avoid haploid consensus sequences, which have heterozygous sites phased at random. In case the analytical integration algorithm is computationally unfeasible, computational phasing prior to population genomic analyses is an acceptable alternative. [BPP; introgression; multispecies coalescent; phase; species tree.]« less

Abstract Spiny lizards in the genus Sceloporus are a model system among squamate reptiles for studies of chromosomal evolution. While most pleurodont iguanians retain an ancestral karyotype formula of 2n = 36 chromosomes, Sceloporus exhibits substantial karyotype variation ranging from 2n =  22 to 46 chromosomes. We present two annotated chromosome-scale genome assemblies for the Plateau Fence Lizard (Sceloporus tristichus) to facilitate research on the role of pericentric inversion polymorphisms on adaptation and speciation. Based on previous karyotype work using conventional staining, the S. tristichus genome is characterized as 2n =  22 with six pairs of macrochromosomes and five pairs of microchromosomes and a pericentric inversion polymorphism on chromosome 7 that is geographically variable. We provide annotated, chromosome-scale genomes for two lizards located at opposite ends of a dynamic hybrid zone that are each fixed for different inversion polymorphisms. The assembled genomes are 1.84–1.87 Gb (1.72 Gb for scaffolds mapping to chromosomes) with a scaffold N50 of 267.5 Mb. Functional annotation of the genomes resulted in ∼15K predicted gene models. Our assemblies confirmed the presence of a 4.62-Mb pericentric inversion on chromosome 7, which contains 62 annotated coding genes with known functions. In addition, we collected population genomics data using double digest RAD-sequencing for 44 S. tristichus to estimatemore »population structure and phylogeny across the Colorado Plateau. These new genomic resources provide opportunities to perform genomic scans and investigate the formation and spread of pericentric inversions in a naturally occurring hybrid zone.« less