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

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

Pairwise <i>F_ST</i> measured between STRUCTURAMA-inferred populations with nDNA.

<p>Pairwise <i>F_ST</i> measured between STRUCTURAMA-inferred populations with nDNA.</p

Pairwise distances within populations.

<p>A: Tamura-Nei corrected distance within each mitochondrial clade. B: Average p-distance across nine nuclear loci within each STRUCTURAMA-inferred population.</p

Mismatch distributions.

<p>The frequency distribution of nDNA polymorphisms within STRUCTURAMA-inferred populations calculated with the concatenated dataset in Arlequin. X-axes are in number of differences and Y-axes are in number of observations. Blue diamonds represent the observed data, green triangles and red squares represent upper and lower bounds expected under a model of expansion, respectively. P-values of the raggedness index for each analysis are given. A: Gulf-Atlantic. B: Suwannee. C: Carolinas. D: Everglades.</p

Geographic distribution of genetic populations.

<p>Colored shapes indicate the extent and boundaries of each inferred population. 3A shows the distribution of the four major mitochondrial clades: NC (yellow), Gulf/Atlantic (green), Suwannee (blue), and Everglades (magenta). The orange arrow indicates location of the Tennessee subpopulation. The yellow arrow indicates one individual in central FL that clusters with the NC clade. 3B shows the geographic distribution of the STRUCTURAMA-inferred genetic clusters. Color key is the same as 3A, except the yellow shape denotes the range of the Carolinas population inferred by nDNA versus the NC clade inferred by mtDNA. The yellow arrow points to the same individual in 3A, which clusters with the Suwannee population in the STRUCTURAMA analysis.</p

Summary statistics for each mtDNA clade and STRUCTURAMA-inferred group.

<p>Summary statistics for each mtDNA clade and STRUCTURAMA-inferred group.</p

Neighbor-joining tree derived from pairwise <i>F_ST</i> of green anole subpopulations.

<p>Colors indicate the mitochondrial clade to which individuals in the subpopulation belong: Gulf/Atlantic (green), NC (yellow), Suwannee (blue) and Everglades (magenta).</p

Estimates of effective population size obtained from the skyline plots implemented in BEAST.

<p>HPD  =  highest posterior density.</p

Analysis of Molecular Variance (AMOVA).

<p>Analysis of Molecular Variance (AMOVA).</p

Phylogenetic reconstruction of the ND2 mitochondrial region.

<p>The most likely tree derived from the rapid bootstrap method (RBS) in RaxML is shown; the topologies of three methods (RBS, full likelihood, and Bayesian inference) were highly concordant. Posterior probabilities are given above important nodes; below nodes are the bootstrap values from RBS before the slash and from the full ML analysis after the slash. Nodes with 100% support in all three analyses are indicated with a 1. Outgroups (<i>A. isolepis</i>, <i>A. altitudinalis</i> and <i>A. porcatus</i>) are not shown. The four major clades (Suwannee, North Carolina, Gulf-Atlantic, and Everglades) are indicated with large brackets on the right. The Tennessee minor clade is shown, nested within the Gulf-Atlantic lineage. Two samples from central FL that clustered closer to the North Carolina clade are indicated with a black arrow.</p