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      Tip-dating and homoplasy: reconciling the shallow molecular divergences of modern gharials with their long fossil record

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      Proceedings of the Royal Society B: Biological Sciences

      The Royal Society

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          Abstract

          <p class="first" id="d702841e180">Simultaneously analysing morphological, molecular and stratigraphic data suggests a potential resolution to a major remaining inconsistency in crocodylian evolution. The ancient, long-snouted thoracosaurs have always been placed near the Indian gharial <i>Gavialis</i>, but their antiquity ( <i>ca</i> 72 Ma) is highly incongruous with genomic evidence for the young age of the <i>Gavialis</i> lineage ( <i>ca</i> 40 Ma). We reconcile this contradiction with an updated morphological dataset and novel analysis, and demonstrate that thoracosaurs are an ancient iteration of long-snouted stem crocodylians unrelated to modern gharials. The extensive similarities between thoracosaurs and <i>Gavialis</i> are shown to be an almost ‘perfect storm’ of homoplasy, combining convergent adaptions to fish-eating, as well resemblances between genuinely primitive traits (thoracosaurs) and atavisms ( <i>Gavialis</i>). Phylogenetic methods that ignore stratigraphy (parsimony and undated Bayesian methods) are unable to tease apart these similarities and invariably unite thoracosaurs and <i>Gavialis.</i> However, tip-dated Bayesian approaches additionally consider the large temporal gap separating ancient (thoracosaurs) and modern ( <i>Gavialis</i>) iterations of similar long-snouted crocodyliforms. These analyses robustly favour a phylogeny which places thoracosaurs basal to crocodylians, far removed from modern gharials, which accordingly are a very young radiation. This phylogenetic uncoupling of ancient and modern gharial-like crocs is more consistent with molecular clock divergence estimates, and also the bulk of the crocodylian fossil record (e.g. all unequivocal gharial fossils are very young). Provided that the priors and models attribute appropriate relative weights to the morphological and stratigraphic signals—an issue that requires investigation—tip-dating approaches are potentially better able to detect homoplasy and improve inferences about phylogenetic relationships, character evolution and divergence dates. </p>

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          Most cited references 21

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          AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics.

          A key element to a successful Markov chain Monte Carlo (MCMC) inference is the programming and run performance of the Markov chain. However, the explicit use of quality assessments of the MCMC simulations-convergence diagnostics-in phylogenetics is still uncommon. Here, we present a simple tool that uses the output from MCMC simulations and visualizes a number of properties of primary interest in a Bayesian phylogenetic analysis, such as convergence rates of posterior split probabilities and branch lengths. Graphical exploration of the output from phylogenetic MCMC simulations gives intuitive and often crucial information on the success and reliability of the analysis. The tool presented here complements convergence diagnostics already available in other software packages primarily designed for other applications of MCMC. Importantly, the common practice of using trace-plots of a single parameter or summary statistic, such as the likelihood score of sampled trees, can be misleading for assessing the success of a phylogenetic MCMC simulation. The program is available as source under the GNU General Public License and as a web application at http://ceb.scs.fsu.edu/awty.
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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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              Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria)

              Background The morphological peculiarities of turtles have, for a long time, impeded their accurate placement in the phylogeny of amniotes. Molecular data used to address this major evolutionary question have so far been limited to a handful of markers and/or taxa. These studies have supported conflicting topologies, positioning turtles as either the sister group to all other reptiles, to lepidosaurs (tuatara, lizards and snakes), to archosaurs (birds and crocodiles), or to crocodilians. Genome-scale data have been shown to be useful in resolving other debated phylogenies, but no such adequate dataset is yet available for amniotes. Results In this study, we used next-generation sequencing to obtain seven new transcriptomes from the blood, liver, or jaws of four turtles, a caiman, a lizard, and a lungfish. We used a phylogenomic dataset based on 248 nuclear genes (187,026 nucleotide sites) for 16 vertebrate taxa to resolve the origins of turtles. Maximum likelihood and Bayesian concatenation analyses and species tree approaches performed under the most realistic models of the nucleotide and amino acid substitution processes unambiguously support turtles as a sister group to birds and crocodiles. The use of more simplistic models of nucleotide substitution for both concatenation and species tree reconstruction methods leads to the artefactual grouping of turtles and crocodiles, most likely because of substitution saturation at third codon positions. Relaxed molecular clock methods estimate the divergence between turtles and archosaurs around 255 million years ago. The most recent common ancestor of living turtles, corresponding to the split between Pleurodira and Cryptodira, is estimated to have occurred around 157 million years ago, in the Upper Jurassic period. This is a more recent estimate than previously reported, and questions the interpretation of controversial Lower Jurassic fossils as being part of the extant turtles radiation. Conclusions These results provide a phylogenetic framework and timescale with which to interpret the evolution of the peculiar morphological, developmental, and molecular features of turtles within the amniotes.
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                Author and article information

                Journal
                Proceedings of the Royal Society B: Biological Sciences
                Proc. R. Soc. B
                The Royal Society
                0962-8452
                1471-2954
                June 27 2018
                June 27 2018
                June 27 2018
                June 27 2018
                : 285
                : 1881
                : 20181071
                Article
                10.1098/rspb.2018.1071
                6030529
                30051855
                © 2018

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