Genome-scale data reveal deep lineage divergence and a complex demographic history in the Texas horned lizard (Phrynosoma cornutum) throughout the southwestern and central US

Abstract

The southern US and northern Mexico 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 with evidence of recent admixture. The spatial distribution of populations appears concordant with habitat type, with desert populations in Arizona and New Mexico showing the largest genetic divergence. The mtDNA data also support a divergent desert population, but other relationships differ and suggest mtDNA introgression. Genotype-environmental association analyses support divergence along environmental axes. Demographic analyses support a model of allopatric divergence during the Pleistocene followed by secondary contact and gene flow. These results are consistent with inferred paleo-species distribution models. Our results also indicate that caution is warranted when fitting a multispecies coalescent model without introgression to populations that have exchanged genes throughout their diversification history. In sum, our results support allopatric divergence due to Pleistocene climate change, which was followed by secondary contact and widespread genomic introgression. 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.

Power of Bayesian and Heuristic Tests to Detect Cross-Species Introgression with Reference to Gene Flow in the Tamias quadrivittatus Group of North American Chipmunks

“…The past two decades have seen widespread use of genomic data to infer hybridization or introgression (Mallet et al, 2016). Gene flow has been detected in a variety of species including Arabidopsis (Arnold et al, 2016), butterflies (Martin et al, 2013), corals (Mao et al, 2018), lizards (Finger et al, 2022), birds (Ellegren et al, 2012), and mammals (Kumar et al, 2017;Chan et al, 2013;Shi and Yang, 2018). The studies have considerably enriched our understanding of the evolutionary dynamics of introgressed genes, and the role of introgression in speciation and ecological adaptation (Payseur and Rieseberg, 2016;Martin and Jiggins, 2017).…”

Signals of differential introgression in the genome of natural hybrids of Caribbean anoles

“…Individuals with 60% or greater missing data were excluded, and we removed loci with minor allele frequencies lower than 0.05 (--maf 0.05) and SNPs that were in strong linkage disequilibrium (LD; Rho ≥0.96). LD was estimated using a custom R script developed by Finger et al (2022). When SNPs were found to be in LD, we randomly selected one to include F I G U R E 2 (a) Approximate sampling localities of individuals used to generate the medium-density (N = 73) and high-density (N = 10) SNP datasets used in this study: Anolis pulchellus (A. pulchellus with native mtDNA, dark blue circles, N = 25), hybrids (A. pulchellus with A. krugi mtDNA, light blue circles, N = 23) and A. krugi (red circles, N = 25).…”

Organellar DNA continues to provide a rich source of information in the genomics era

“…All searches excluded review articles. [Colour figure can be viewed at wileyonlinelibrary.com] for evolutionary inference (Crawford et al, 2012;Dam et al, 2017;Eaton & Ree, 2013;Hou et al, 2015;Villaverde et al, 2021;Wagner et al, 2013), although exceptions do exist (Finger et al, 2022;Kato et al, 2020;Zarza et al, 2018). I will argue that this is not an optimal use of resources, given the potential benefits of organellar markers alluded to above.…”

“…Thus, in many cases organellar sequences will not be a reliable indicator of taxonomy, and some nuclear loci will be required. The strength of NGS and methods like ddRADseq and UCEs is that they provide thousands of essentially independent coalescent histories with which researchers can estimate important evolutionary parameters such as species limits, species trees, divergences times, patterns and rates of gene flow, selection, and population size changes (Andrews et al, 2016;Baca et al, 2017;Blair et al, 2019;Bryson et al, 2017;Davey & Blaxter, 2010;Finger et al, 2022).…”