Genetic variation in the green anole lizard (Anolis carolinensis) reveals island refugia and a fragmented Florida during the quaternary

Abstract

The green anole lizard (Anolis carolinensis) is a model organism for behavior and genomics that is native to the southeastern United States. It is currently thought that the ancestors of modern green anoles dispersed to peninsular Florida from Cuba. However, the climatic changes and geological features responsible for the early diversification of A. carolinensis in North America have remained largely unexplored. This is because previous studies (1) differ in their estimates of the divergence times of populations, (2) are based on a single genetic locus or (3) did not test specific hypotheses regarding the geologic and topographic history of Florida. Here we provide a multi-locus study of green anole genetic diversity and find that the Florida peninsula contains a larger number of genetically distinct populations that are more diverse than those on the continental mainland. As a test of the island refugia hypothesis in Pleistocene Florida, we use a coalescent approach to estimate the divergence times of modern green anole lineages. We find that all demographic events occurred during or after the Upper Pliocene and suggest that green anole diversification was driven by population divergence on interglacial island refugia in Florida during the Lower Pleistocene, while the region was often separated from continental North America. When Florida reconnected to the mainland, two separate dispersal events led to the expansion of green anole populations across the Atlantic Seaboard and Gulf Coastal Plain.

Figure 1

Map of Florida sampling localities. Circles indicate localities from Tollis et al. (2012). Boxes (collected by Boissinot lab in 2012) and triangles (obtained from the Hsieh lab in 2012) indicate field localities new to this study.

Figure 2

Majority consensus tree from a phylogenetic analysis conducted in MrBayes3.2 on the mitochondrial NADH-2 region (n=299). The four major mitochondrial lineages of Anolis carolinensis are indicated at right with labeled brackets. Monophyletic groups restricted to mainland North America (the Gulf-Atlantic and North Carolina lineages) are indicated by shaded boxes. The posterior probabilities of important nodes are given. A. porcatus is the only outgroup shown, although A. isolepis and A. altitudinalis were also used in the analysis.

Figure 3

(a) and (b): Geographic distribution of genetic populations of A. carolinensis in Florida. Collecting localities are indicated by black dots. Patterned shapes depict the geographic distribution of mitochondrial lineages (a) and schematic representation of the nDNA clusters (b). Open circles the – Gulf-Atlantic lineage is present in Nassau County near Jacksonville; vertical lines – Suwannee; horizontal lines – Central Florida; black dots – Everglades. (c): Major geologic structural elements of the Florida peninsula. Positive structures of the Ocala, St. John’s, and Brevard platforms are indicated in grey. Lower elements of the Osceola Low and the Okeechobee basin are indicated. Adapted from Lane (1994).

Figure 4

Visualization of the Bayesian clustering analysis, with the most likely number of nDNA genetic clusters K=5 in 158 A. carolinensis samples collected across nine U.S. states. Bottom bar: x-axis represents each individual (arranged by geographic region, labeled below) and shading along the y-axis represents the proportion each individual’s genome derived from one of the K clusters. Top bar: horizontal shading in boxes represent the proportion of each of the five nDNA clusters found in each geographic region. Barplots were produced using the program DISTRUCT (Rosenberg 2004)

Figure 5

Maximum clade credibility tree from a *BEAST analysis using 1 mtDNA and 3 nDNA loci showing the inferred branching order and divergence times for five populations of green anoles and their outgroup A. porcatus. Within A. carolinensis, percent posterior probabilities and divergence time estimates (My = million years) are given to the left and right of each node, respectively.

Figure 6

Hypothesized biogeographic scenario depicting the major events in the history of A. carolinensis in the southeastern United States inferred in this chapter. (1) Green anoles disperse from Cuba to the southern tip of Florida, where the ancestor of modern populations lived near the Plio-Pleistocene boundary. (2) During the Early Pleistocene, physiographic upheaval driven by rising sea levels during glacial cycles cause population fragmentation and divergence. (3) During the late part of the Early Pleistocene, the peninsula connects to the mainland again, and green anole populations living along the Central Atlantic Coast of Florida are able to disperse northwards towards the Carolinas. High elevations along the Appalachian Highlands (lighter shading indicates >750 meters elevation) most likely provided a dispersal barrier westward as unsuitable habitat. (4) During the Middle Pleistocene, populations living along the Gulf Coast of Florida began to colonize watersheds along the Gulf Coastal Plain, resulting in a westward expansion of green anoles across the Mississippi River and into Texas.