Multi-Locus Phylogeographic and Population Genetic Analysis of Anolis carolinensis: Historical Demography of a Genomic Model Species

Abstract

The green anole (Anolis carolinensis) has been widely used as an animal model in physiology and neurobiology but has recently emerged as an important genomic model. The recent sequencing of its genome has shed new light on the evolution of vertebrate genomes and on the process that govern species diversification. Surprisingly, the patterns of genetic diversity within natural populations of this widespread and abundant North American lizard remain relatively unknown. In the present study, we use 10 novel nuclear DNA sequence loci (N = 62 to 152) and one mitochondrial locus (N = 226) to delimit green anole populations and infer their historical demography. We uncovered four evolutionarily distinct and geographically restricted lineages of green anoles using phylogenetics, Bayesian clustering, and genetic distance methods. Molecular dating indicates that these lineages last shared a common ancestor ∼2 million years ago. Summary statistics and analysis of the frequency distributions of DNA polymorphisms strongly suggest range-wide expansions in population size. Using Bayesian Skyline Plots, we inferred the timing of population size expansions, which differ across lineages, and found evidence for a relatively recent and rapid westward expansion of green anoles across the Gulf Coastal Plain during the mid-Pleistocene. One surprising result is that the distribution of genetic diversity is not consistent with a latitudinal shift caused by climatic oscillations as is observed for many co-distributed taxa. This suggests that the most recent Pleistocene glacial cycles had a limited impact on the geographic distribution of the green anole at the northern limits of its range.

Diversification in wild populations of the model organism Anolis carolinensis: A genome‐wide phylogeographic investigation

“…We sampled 42 A. carolinensis individuals from 26 localities across its distributional range (Figure 2a; Table S1) encompassing the five major clades identified in previous molecular work (Campbell‐Staton et al., 2012; Tollis & Boissinot, 2014; Tollis et al., 2012). Individuals of both A. porcatus and A. sagrei were used as outgroups.…”

“…Individuals of both A. porcatus and A. sagrei were used as outgroups. All samples were collected for previous studies (Tollis & Boissinot, 2014; Tollis et al., 2012). For the current sequencing experiment, genomic DNA was extracted via proteinase K digestion followed by purification with the Promega Wizard Genomic DNA Purification standard protocol and elution in TE buffer.…”

“…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.…”

“…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.…”