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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.

SUBMITTER: Tollis M

PROVIDER: S-EPMC4778398 | biostudies-literature | 2014 Feb

REPOSITORIES: biostudies-literature

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

Tollis Marc M Boissinot Stéphane S

Genetica 20131231 1

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 tim ...[more]

PMID: 24379168

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Project description:In allopatric species, reproductive isolation evolves through the accumulation of genetic incompatibilities. The degree of divergence required for complete reproductive isolation is highly variable across taxa, which makes the outcome of secondary contact between allopatric species unpredictable. Since before the Pliocene, two species of Anolis lizards, Anolis carolinensis and Anolis porcatus, have been allopatric, yet this period of independent evolution has not led to substantial species-specific morphological differentiation, and therefore, they might not be reproductively isolated. In this study, we determined the genetic consequences of localized, secondary contact between the native green anole, A. carolinensis, and the introduced Cuban green anole, A. porcatus, in South Miami. Using 18 microsatellite markers, we found that the South Miami population formed a genetic cluster distinct from both parental species. Mitochondrial DNA revealed maternal A. porcatus ancestry for 35% of the individuals sampled from this population, indicating a high degree of cytonuclear discordance. Thus, hybridization with A. porcatus, not just population structure within A. carolinensis, may be responsible for the genetic distinctiveness of this population. Using tree-based maximum-likelihood analysis, we found support for a more recent, secondary introduction of A. porcatus to Florida. Evidence that ~33% of the nuclear DNA resulted from a secondary introduction supports the hybrid origin of the green anole population in South Miami. We used multiple lines of evidence and multiple genetic markers to reconstruct otherwise cryptic patterns of species introduction and hybridization. Genetic evidence for a lack of reproductive isolation, as well as morphological similarities between the two species, supports revising the taxonomy of A. carolinensis to include A. porcatus from western Cuba. Future studies should target the current geographic extent of introgression originating from the past injection of genetic material from Cuban green anoles and determine the consequences for the evolutionary trajectory of green anole populations in southern Florida.

Project description:Protemics of anolis carolinensis tails undergoing regeneration. As amniote vertebrates, lizards are the most closely related organisms to humans capable of appendage regeneration. Lizards can autotomize, or release their tails as a means of predator evasion, and subsequently regenerate a functional replacement. Green anoles (Anolis carolinensis) can regenerate their tails through a process that involves differential expression of hundreds of genes, which has previously been analyzed by transcriptomic and microRNA analysis. To investigate protein expression in regenerating tissue, we performed whole proteomic analysis of regenerating tail tip and base. This is the first proteomic data set available for the green anole lizard. We identified 976 proteins only in the regenerating tail base, 796 only in the tail tip, and 874 in both tip and base. For 90% of these proteins in these tissues, we were able to assign a clear orthology to gene models in either the Ensembl or NCBI databases. For 20 proteins in the tail base (2.5%), 7 proteins in the tail tip (0.9%), and 7 proteins in both regions (0.8%), the gene model in Ensembl and NCBI matched an uncharacterized protein, confirming that these predictions are present in the proteome. Ontology and pathways analysis of proteins expressed in the regenerating tail base identified categories including actin filament-based process, ncRNA metabolism, regulation of phosphatase activity, small GTPase mediated signal transduction, and cellular component organization or biogenesis. Analysis of proteins expressed in the tail tip identified categories including regulation of organelle organization, regulation of protein localization, ubiquitin-dependent protein catabolism, small GTPase mediated signal transduction, morphogenesis of epithelium, and regulation of biological quality. These proteomic findings confirm pathways and gene families activated in tail regeneration in the green anole as well as identify uncharacterized proteins whose role in regrowth remains to be revealed.

Project description:BackgroundTandem amino acid repeats are characterised by the consecutive recurrence of a single amino acid. They exhibit high rates of length mutations in addition to point mutations and have been proposed to be involved in genetic plasticity. Squamate reptiles (lizards and snakes) diversify in both morphology and physiology. The underlying mechanism is yet to be understood. In a previous phylogenomic analysis of reptiles, the density of tandem repeats in an anole lizard diverged heavily from that of the other reptiles. To gain further insight into the tandem amino acid repeats in squamates, we analysed the repeat content in the green anole (Anolis carolinensis) proteome and compared the amino acid repeats in a large orthologous protein data set from six vertebrates (the Western clawed frog, the green anole, the Chinese softshell turtle, the zebra finch, mouse and human).ResultsOur results revealed that the number of amino acid repeats in the green anole exceeded those found in the other five species studied. Species-only repeats were found in high proportion in the green anole but not in the other five species, suggesting that the green anole had gained many amino acid repeats in either the Anolis or the squamate lineage. Since the amino acid repeat containing genes in the green anole were highly enriched in genes related to transcription and development, an important family of developmental genes, i.e., the Hox family, was further studied in a wide collection of squamates. Abundant amino acid repeats were also observed, implying the general high tolerance of amino acid repeats in squamates. A particular enrichment of amino acid repeats was observed in the central class Hox genes that are known to be responsible for defining cervical to lumbar regions.ConclusionsOur study suggests that the abundant amino acid repeats in the green anole, and possibly in other squamates, may play a role in increasing the genetic variability, and contribute to the evolutionary diversity of this clade.

Dataset Information

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

Publications

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

Similar Datasets

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