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Multi-locus phylogeographic and population genetic analysis of Anolis carolinensis: historical demography of a genomic model species.

Tollis M, Ausubel G, Ghimire D, Boissinot S - PLoS ONE (2012)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, Queens College, City University of New York, Flushing, New York, United States of America.

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.

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Geographic distribution of genetic populations.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.
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pone-0038474-g003: Geographic distribution of genetic populations.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.

Mentions: All phylogenetic analyses yielded highly concordant topologies. The most likely tree from the RBS ML analysis of the mtDNA is shown in Figure 2, with posterior probabilities (pp) and bootstrap (bs) values shown above and below important nodes, respectively. The monophyly of A. carolinensis is strongly supported (1.0 bs and pp). As in the preliminary BI analysis, the final BI analysis recovered four major mtDNA clades with 100% pp. These clades are strongly correlated with geographic region (Figure 3A) and consist of (1) a lineage endemic to the Gulf coast region of FL in or around the Suwannee River drainage system (the “Suwannee” clade); (2) a group limited to anoles from the southern tip of the FL peninsula (the “Everglades” clade); (3) a NC clade and (4) a large clade including samples from all other localities ranging from the Atlantic coast of northern FL across the Gulf Coastal Plain to TX (the “Gulf-Atlantic” clade). Relationships within the Gulf-Atlantic clade could not be well resolved, with individuals from disparate geographic regions often clustering together with extremely low posterior support. One interesting well-supported minor mtDNA clade within the major Gulf-Atlantic clade consists of individuals collected from various localities on the western side of the Smoky Mountains in eastern TN. An unexpected result was the occurrence of two ND2 sequences from FL (one collected by us and one from GenBank) clustering just outside the NC clade to form a monphyletic group, and we address this below and in the Discussion section.


Multi-locus phylogeographic and population genetic analysis of Anolis carolinensis: historical demography of a genomic model species.

Tollis M, Ausubel G, Ghimire D, Boissinot S - PLoS ONE (2012)

Geographic distribution of genetic populations.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.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3369884&req=5

pone-0038474-g003: Geographic distribution of genetic populations.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.
Mentions: All phylogenetic analyses yielded highly concordant topologies. The most likely tree from the RBS ML analysis of the mtDNA is shown in Figure 2, with posterior probabilities (pp) and bootstrap (bs) values shown above and below important nodes, respectively. The monophyly of A. carolinensis is strongly supported (1.0 bs and pp). As in the preliminary BI analysis, the final BI analysis recovered four major mtDNA clades with 100% pp. These clades are strongly correlated with geographic region (Figure 3A) and consist of (1) a lineage endemic to the Gulf coast region of FL in or around the Suwannee River drainage system (the “Suwannee” clade); (2) a group limited to anoles from the southern tip of the FL peninsula (the “Everglades” clade); (3) a NC clade and (4) a large clade including samples from all other localities ranging from the Atlantic coast of northern FL across the Gulf Coastal Plain to TX (the “Gulf-Atlantic” clade). Relationships within the Gulf-Atlantic clade could not be well resolved, with individuals from disparate geographic regions often clustering together with extremely low posterior support. One interesting well-supported minor mtDNA clade within the major Gulf-Atlantic clade consists of individuals collected from various localities on the western side of the Smoky Mountains in eastern TN. An unexpected result was the occurrence of two ND2 sequences from FL (one collected by us and one from GenBank) clustering just outside the NC clade to form a monphyletic group, and we address this below and in the Discussion section.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, Queens College, City University of New York, Flushing, New York, United States of America.

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.

Show MeSH