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      Adaptive Color Polymorphism and Unusually High Local Genetic Diversity in the Side-Blotched Lizard, Uta stansburiana

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          Abstract

          Recently, studies of adaptive color variation have become popular as models for examining the genetics of natural selection. We examined color pattern polymorphism and genetic variation in a population of side-blotched lizards ( Uta stansburiana) that is found in habitats with both dark (lava) and light colored (granite) substrates. We conducted a limited experiment for adult phenotypic plasticity in laboratory conditions. We recorded both substrate and lizard color patterns in the field to determine whether lizards tended to match their substrate. Finally we examined genetic variation in a gene ( melanocortin 1 receptor) that has been shown to affect lizard color in other species and in a presumably neutral gene (mitochondrial cytochrome b). Populations were sampled in the immediate area of the lava flows as well as from a more distant site to examine the role of population structure. Our captive Uta did not change color to match their background. We show that side-blotched lizards tend to match the substrate on which it was caught in the field and that variation in the melanocortin 1 receptor gene does not correlate well with color pattern in this population. Perhaps the most remarkable result is that this population of side-blotched lizards shows extremely high levels of variation at both genetic markers, in the sense of allele numbers, with relatively low levels of between-allele sequence variation. Genetic variation across this small region was as great or greater than that seen in samples of pelagic fish species collected worldwide. Statistical analysis of genetic variation suggests rapid population expansion may be responsible for the high levels of variation.

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          A single amino acid mutation contributes to adaptive beach mouse color pattern.

          Natural populations of beach mice exhibit a characteristic color pattern, relative to their mainland conspecifics, driven by natural selection for crypsis. We identified a derived, charge-changing amino acid mutation in the melanocortin-1 receptor (Mc1r) in beach mice, which decreases receptor function. In genetic crosses, allelic variation at Mc1r explains 9.8% to 36.4% of the variation in seven pigmentation traits determining color pattern. The derived Mc1r allele is present in Florida's Gulf Coast beach mice but not in Atlantic coast mice with similar light coloration, suggesting that different molecular mechanisms are responsible for convergent phenotypic evolution. Here, we link a single mutation in the coding region of a pigmentation gene to adaptive quantitative variation in the wild.
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            Theory and speciation.

            The study of speciation has become one of the most active areas of evolutionary biology, and substantial progress has been made in documenting and understanding phenomena ranging from sympatric speciation and reinforcement to the evolutionary genetics of postzygotic isolation. This progress has been driven largely by empirical results, and most useful theoretical work has concentrated on making sense of empirical patterns. Given the complexity of speciation, mathematical theory is subordinate to verbal theory and generalizations about data. Nevertheless, mathematical theory can provide a useful classification of verbal theories; can help determine the biological plausibility of verbal theories; can determine whether alternative mechanisms of speciation are consistent with empirical patterns; and can occasionally provide predictions that go beyond empirical generalizations. We discuss recent examples of progress in each of these areas.
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              Adaptive reptile color variation and the evolution of the Mc1r gene.

              The wealth of information on the genetics of pigmentation and the clear fitness consequences of many pigmentation phenotypes provide an opportunity to study the molecular basis of an ecologically important trait. The melanocortin-1 receptor (Mc1r) is responsible for intraspecific color variation in mammals and birds. Here, we study the molecular evolution of Mc1r and investigate its role in adaptive intraspecific color differences in reptiles. We sequenced the complete Mc1r locus in seven phylogenetically diverse squamate species with melanic or blanched forms associated with different colored substrates or thermal environments. We found that patterns of amino acid substitution across different regions of the receptor are similar to the patterns seen in mammals, suggesting comparable levels of constraint and probably a conserved function for Mc1r in mammals and reptiles. We also found high levels of silent-site heterozygosity in all species, consistent with a high mutation rate or large long-term effective population size. Mc1r polymorphisms were strongly associated with color differences in Holbrookia maculata and Aspidoscelis inornata. In A. inornata, several observations suggest that Mc1r mutations may contribute to differences in color: (1) a strong association is observed between one Mc1r amino acid substitution and dorsal color; (2) no significant population structure was detected among individuals from these populations at the mitochondrial ND4 gene; (3) the distribution of allele frequencies at Mc1r deviates from neutral expectations; and (4) patterns of linkage disequilibrium at Mc1r are consistent with recent selection. This study provides comparative data on a nuclear gene in reptiles and highlights the utility of a candidate-gene approach for understanding the evolution of genes involved in vertebrate adaptation.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                25 October 2012
                : 7
                : 10
                : e47694
                Affiliations
                [1]Department of Biology, San Francisco State University, San Francisco, California, United States of America
                Institut de Biologia Evolutiva - Universitat Pompeu Fabra, Spain
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SM EJR. Performed the experiments: SM EP EJR. Analyzed the data: SM EJR. Contributed reagents/materials/analysis tools: SM EJR. Wrote the paper: SM EJR.

                [¤]

                Current address: School of Biological Sciences, Washington State University, Pullman, Washington, United States of America

                Article
                PONE-D-12-20575
                10.1371/journal.pone.0047694
                3485026
                23133520
                f5ac2196-f6fb-4615-b89d-f98c327a6b3f
                Copyright @ 2012

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 12 July 2012
                : 17 September 2012
                Page count
                Pages: 11
                Funding
                This work was supported by Sigma Xi Grant in Aid of Research, SFSU IRA, SFSU Center for Computing in Life Sciences. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Evolutionary Biology
                Evolutionary Processes
                Adaptation
                Genetic Drift
                Forms of Evolution
                Divergent Evolution
                Population Genetics
                Effective Population Size
                Gene Flow
                Gene Pool
                Genetic Drift
                Natural Selection
                Evolutionary Genetics
                Zoology
                Herpetology

                Uncategorized
                Uncategorized

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