1 Introduction

A current necessity in evolutionary biology is to understand how evolutionary history shapes natural variation in model organisms for complex traits (Gasch, Payseur, & Pool, 2016). The green anole lizard (Anolis carolinensis) was the first nonavian reptile to have a complete genome sequence (Alföldi et al., 2011) and is an indispensable laboratory model for biomedical fields such as reproductive endocrinology (Lovern, Holmes, & Wade, 2004; Wade, 2012) and appendage regeneration (Hutchins et al., 2014). However, unlike studies using established models such as the house mouse (Mus musculus), which rely on inbred strains, green anole laboratory protocols are based on wild‐caught individuals. This is despite the fact that with a natural range across the southeastern United States, A. carolinensis exhibits wide geographic variation in morphology (Jaffe, Campbell‐Staton, & Losos, 2016) and physiology (Goodman et al., 2013), and the connection between genetic and phenotypic diversity in the species remains unknown.

More generally, the distribution of A. carolinensis overlaps with a suite of species with phylogeographic structure in the southeastern United States (for a review, see Soltis et al., 2006). In this region, terrestrial species’ genetic structure generally coincides with barriers such as the Appalachian Mountains and several large river systems. In many of these taxa, genetic structure was hypothesized to be a consequence of divergence in allopatry during the Last Glacial Maximum followed by subsequent range expansions out of refugia (Soltis et al., 2006). In this context, resolving the phylogeographic history of A. carolinensis would provide an additional reference to the biogeographic history of this region. Therefore, in order to better develop A. carolinensis as a model in biomedical and genomic research, as well as compare its evolutionary history with broader biogeographic patterns, a clear picture of its phylogeographic and demographic history is necessary.

The evolutionary history of A. carolinensis has yet to be fully resolved, due to differing conclusions that are based on only a few genetic markers. The species is phylogenetically nested within the Cuban green anole A. porcatus, and there is agreement that it originated in Florida after overwater dispersal from Cuba (Buth, Gorman, & Leib, 1980; Glor, Losos, & Larson, 2005). Recent analyses of mitochondrial DNA (mtDNA) fragments and small numbers of nuclear DNA loci agree that Florida contains most of green anole genetic diversity, and the intrapopulational distributions of DNA polymorphisms suggest population size expansions on the continental mainland (Campbell‐Staton et al., 2012; Tollis, Ausubel, Ghimire, & Boissinot, 2012; Tollis & Boissinot, 2014). Based on these conclusions, it was suggested that early green anole divergence was fueled by vicariance across Pleistocene island refugia on the Florida peninsula, followed by more recent dispersal both northwards along the Atlantic seaboard and west across the Gulf Coastal Plain (Tollis & Boissinot, 2014).

Previous phylogeographic analyses of A. carolinensis identified five geographically structured clades across the species range: three in Florida and two out of Florida (Campbell‐Staton et al., 2012; Tollis & Boissinot, 2014; Tollis et al., 2012). However, these studies identified conflicting and poorly supported relationships among the clades. All three studies found a sister relationship between localities in the Carolinas (North and South) and eastern Florida (Figure 1). Phylogenies based on mtDNA identified western and northwestern localities in Florida as sister to all other populations (Figure 1a; Campbell‐Staton et al., 2012; Tollis et al., 2012), while southern Florida (i.e., Everglades) localities were sister to all other populations using a species tree analysis (Figure 1b, Tollis & Boissinot, 2014). In both trees (Figures 1a,b), all but two clades had different sister relationships. Thus, the branching order of divergence events and true relatedness of subpopulations within A. carolinensis remain unresolved, obscuring the potential effects of evolutionary history on biomedical studies that may include green anoles from different sampling localities. Therefore, increased effort to resolve relationships between A. carolinensis subpopulations with a larger sampling of genetic loci is needed.

Figure 1 Open in figure viewer PowerPoint Phylogenies estimated from previous studies, simplified to the five main genetic clusters for clarity. Group names refer to the same regions and genetic clusters as shown in Figures 2 5 , with the exception of the Carolinas. In the mtDNA studies (a), South Carolina was in the Gulf‐Atlantic clade, while North Carolina had its own clade. In the multilocus tree (b), the Carolinas clade was mostly North Carolina, with some individuals of South Carolina

Recently developed methodologies such as restriction site‐associated DNA sequencing (RAD‐seq, Miller et al., 2007) and target capture using ultraconserved elements (UCEs, Faircloth et al., 2012) or anchored hybrid enrichment (AHE, Lemmon, Emme, & Lemmon, 2012) now allow researchers to obtain reduced representation genomic coverage across many individuals. All three types of data collection have been shown to be appropriate for phylogeographic‐level studies of vertebrates, including RAD‐seq (Manthey & Moyle, 2015), UCEs (Smith et al., 2013), and AHE (Brandley et al., 2015), suggesting these methods’ ability to resolve the evolutionary history of A. carolinensis. Here, we used more than 500 genome‐wide loci collected via AHE with the following goals: (1) clarify the evolutionary relationships of previously identified clades in A. carolinensis, (2) explore patterns and trends of genetic diversity and differentiation within and among lineages, (3) elucidate the demographic history and timing of diversification within the species, and (4) compare the phylogeographic patterns found in A. carolinensis with other species from the southeastern United States.