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      Integrated Analyses Resolve Conflicts over Squamate Reptile Phylogeny and Reveal Unexpected Placements for Fossil Taxa

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          Abstract

          Squamate reptiles (lizards and snakes) are a pivotal group whose relationships have become increasingly controversial. Squamates include >9000 species, making them the second largest group of terrestrial vertebrates. They are important medicinally and as model systems for ecological and evolutionary research. However, studies of squamate biology are hindered by uncertainty over their relationships, and some consider squamate phylogeny unresolved, given recent conflicts between molecular and morphological results. To resolve these conflicts, we expand existing morphological and molecular datasets for squamates (691 morphological characters and 46 genes, for 161 living and 49 fossil taxa, including a new set of 81 morphological characters and adding two genes from published studies) and perform integrated analyses. Our results resolve higher-level relationships as indicated by molecular analyses, and reveal hidden morphological support for the molecular hypothesis (but not vice-versa). Furthermore, we find that integrating molecular, morphological, and paleontological data leads to surprising placements for two major fossil clades (Mosasauria and Polyglyphanodontia). These results further demonstrate the importance of combining fossil and molecular information, and the potential problems of estimating the placement of fossil taxa from morphological data alone. Thus, our results caution against estimating fossil relationships without considering relevant molecular data, and against placing fossils into molecular trees (e.g. for dating analyses) without considering the possible impact of molecular data on their placement.

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          Most cited references 24

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          A Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera

          Phylogenies are usually dated by calibrating interior nodes against the fossil record. This relies on indirect methods that, in the worst case, misrepresent the fossil information. Here, we contrast such node dating with an approach that includes fossils along with the extant taxa in a Bayesian total-evidence analysis. As a test case, we focus on the early radiation of the Hymenoptera, mostly documented by poorly preserved impression fossils that are difficult to place phylogenetically. Specifically, we compare node dating using nine calibration points derived from the fossil record with total-evidence dating based on 343 morphological characters scored for 45 fossil (4--20 complete) and 68 extant taxa. In both cases we use molecular data from seven markers (∼5 kb) for the extant taxa. Because it is difficult to model speciation, extinction, sampling, and fossil preservation realistically, we develop a simple uniform prior for clock trees with fossils, and we use relaxed clock models to accommodate rate variation across the tree. Despite considerable uncertainty in the placement of most fossils, we find that they contribute significantly to the estimation of divergence times in the total-evidence analysis. In particular, the posterior distributions on divergence times are less sensitive to prior assumptions and tend to be more precise than in node dating. The total-evidence analysis also shows that four of the seven Hymenoptera calibration points used in node dating are likely to be based on erroneous or doubtful assumptions about the fossil placement. With respect to the early radiation of Hymenoptera, our results suggest that the crown group dates back to the Carboniferous, ∼309 Ma (95% interval: 291--347 Ma), and diversified into major extant lineages much earlier than previously thought, well before the Triassic. [Bayesian inference; fossil dating; morphological evolution; relaxed clock; statistical phylogenetics.]
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            A Concern for Evidence and a Phylogenetic Hypothesis of Relationships Among Epicrates (Boidae, Serpentes)

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              Assembling the Squamate Tree of Life: Perspectives from the Phenotype and the Fossil Record

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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                24 March 2015
                2015
                : 10
                : 3
                Affiliations
                [1 ]Department of Biology, San Diego State University, San Diego, California, 92182, United States of America
                [2 ]Laboratories of Analytical Biology, Smithsonian Institution, 10th & Constitution Aves. NW, Washington, D.C., 20560, United States of America
                [3 ]Department of Biology, University of Mississippi, Box 1848, Mississippi, 38677, United States of America
                [4 ]Department of Biology and Bean Life Science Museum, Brigham Young University, Provo, Utah, 84602, United States of America
                [5 ]Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, 85721, United States of America
                Penn State University, UNITED STATES
                Author notes

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

                Conceived and designed the experiments: TWR JJW. Performed the experiments: TWR DGM PLW JJW. Analyzed the data: TWR DGM PLW JJW. Contributed reagents/materials/analysis tools: TWR DGM PLW JJW. Wrote the paper: TWR TMT DGM BPN PLW JWS JJW.

                Article
                PONE-D-14-44008
                10.1371/journal.pone.0118199
                4372529
                25803280

                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

                Page count
                Figures: 1, Tables: 1, Pages: 22
                Product
                Funding
                This project was supported by a United States National Science Foundation grant, with awards to T.W.R. (EF 0334967), J.W.S. (EF 0334966) and J.J.W. (EF 0334923). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All data are available on Dryad (doi: 10.5061/dryad.38417).

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