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      Phylogeny, Evolution and Classification of Gall Wasps: The Plot Thickens

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          Abstract

          Gall wasps (Cynipidae) represent the most spectacular radiation of gall-inducing insects. In addition to true gall formers, gall wasps also include phytophagous inquilines, which live inside the galls induced by gall wasps or other insects. Here we present the first comprehensive molecular and total-evidence analyses of higher-level gall wasp relationships. We studied more than 100 taxa representing a rich selection of outgroups and the majority of described cynipid genera outside the diverse oak gall wasps (Cynipini), which were more sparsely sampled. About 5 kb of nucleotide data from one mitochondrial (COI) and four nuclear (28S, LWRh, EF1alpha F1, and EF1alpha F2) markers were analyzed separately and in combination with morphological and life-history data. According to previous morphology-based studies, gall wasps evolved in the Northern Hemisphere and were initially herb gallers. Inquilines originated once from gall inducers that lost the ability to initiate galls. Our results, albeit not conclusive, suggest a different scenario. The first gall wasps were more likely associated with woody host plants, and there must have been multiple origins of gall inducers, inquilines or both. One possibility is that gall inducers arose independently from inquilines in several lineages. Except for these surprising results, our analyses are largely consistent with previous studies. They confirm that gall wasps are conservative in their host-plant preferences, and that herb-galling lineages have radiated repeatedly onto the same set of unrelated host plants. We propose a revised classification of the family into twelve tribes, which are strongly supported as monophyletic across independent datasets. Four are new: Aulacideini, Phanacidini, Diastrophini and Ceroptresini. We present a key to the tribes and discuss their morphological and biological diversity. Until the relationships among the tribes are resolved, the origin and early evolution of gall wasps will remain elusive.

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          Most cited references 15

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          Bayesian phylogenetic analysis of combined data.

          The recent development of Bayesian phylogenetic inference using Markov chain Monte Carlo (MCMC) techniques has facilitated the exploration of parameter-rich evolutionary models. At the same time, stochastic models have become more realistic (and complex) and have been extended to new types of data, such as morphology. Based on this foundation, we developed a Bayesian MCMC approach to the analysis of combined data sets and explored its utility in inferring relationships among gall wasps based on data from morphology and four genes (nuclear and mitochondrial, ribosomal and protein coding). Examined models range in complexity from those recognizing only a morphological and a molecular partition to those having complex substitution models with independent parameters for each gene. Bayesian MCMC analysis deals efficiently with complex models: convergence occurs faster and more predictably for complex models, mixing is adequate for all parameters even under very complex models, and the parameter update cycle is virtually unaffected by model partitioning across sites. Morphology contributed only 5% of the characters in the data set but nevertheless influenced the combined-data tree, supporting the utility of morphological data in multigene analyses. We used Bayesian criteria (Bayes factors) to show that process heterogeneity across data partitions is a significant model component, although not as important as among-site rate variation. More complex evolutionary models are associated with more topological uncertainty and less conflict between morphology and molecules. Bayes factors sometimes favor simpler models over considerably more parameter-rich models, but the best model overall is also the most complex and Bayes factors do not support exclusion of apparently weak parameters from this model. Thus, Bayes factors appear to be useful for selecting among complex models, but it is still unclear whether their use strikes a reasonable balance between model complexity and error in parameter estimates.
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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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              Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo.

              A common problem in molecular phylogenetics is choosing a model of DNA substitution that does a good job of explaining the DNA sequence alignment without introducing superfluous parameters. A number of methods have been used to choose among a small set of candidate substitution models, such as the likelihood ratio test, the Akaike Information Criterion (AIC), the Bayesian Information Criterion (BIC), and Bayes factors. Current implementations of any of these criteria suffer from the limitation that only a small set of models are examined, or that the test does not allow easy comparison of non-nested models. In this article, we expand the pool of candidate substitution models to include all possible time-reversible models. This set includes seven models that have already been described. We show how Bayes factors can be calculated for these models using reversible jump Markov chain Monte Carlo, and apply the method to 16 DNA sequence alignments. For each data set, we compare the model with the best Bayes factor to the best models chosen using AIC and BIC. We find that the best model under any of these criteria is not necessarily the most complicated one; models with an intermediate number of substitution types typically do best. Moreover, almost all of the models that are chosen as best do not constrain a transition rate to be the same as a transversion rate, suggesting that it is the transition/transversion rate bias that plays the largest role in determining which models are selected. Importantly, the reversible jump Markov chain Monte Carlo algorithm described here allows estimation of phylogeny (and other phylogenetic model parameters) to be performed while accounting for uncertainty in the model of DNA substitution.
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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
                20 May 2015
                2015
                : 10
                : 5
                Affiliations
                [1 ]Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden
                [2 ]Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain
                [3 ]Systematic Entomology Lab, USDA, c/o Smithsonian Institution, Washington DC, United States of America
                [4 ]Department of Biological Sciences, Eastern Illinois University, Charleston, IL, United States of America
                [5 ]Swedish Species Information Centre, Swedish University of Agricultural Sciences, Uppsala, Sweden
                [6 ]Bioinformatics Infrastructure for Life Sciences, Linköping University, Linköping, Sweden
                Institut National de la Recherche Agronomique (INRA), FRANCE
                Author notes

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

                Conceived and designed the experiments: FR JAAN. Analyzed the data: FR JAAN. Contributed reagents/materials/analysis tools: FR JAAN JLNA MB ZL JL. Wrote the paper: FR JAAN JLNA MB JL ZL. DNA sequencing: JAAN JLNA MB. Coding of morphology and biology: JLNA FR JL. Initial draft of taxonomic section and illustrated key: JLNA.

                Article
                PONE-D-14-21986
                10.1371/journal.pone.0123301
                4439057
                25993346

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication

                Page count
                Figures: 18, Tables: 4, Pages: 40
                Product
                Funding
                This work received support from: 2011-5622, Swedish Research Council ( http://vr.se): FR. CGL-2009-10111 and CGL-2010-15786, Spanish Ministry of Science and Innovation ( http://www.idi.mineco.gob.es): JLNA. Kalbfleisch Fellowship, American Museum of Natural History ( http://www.amnh.org): ZL. Boyd Scholarship, The Field Museum ( http://www.fieldmuseum.org): ZL. Training Grant #1K12 Gm00708, National Science Foundation ( http://www.nsf.gov): ZL. DEB-0337220 (HymAToL), National Science Foundation ( http://www.nsf.gov): FR MB. 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
                Data are available from GenBank (accesion numbers in Table S1), from TreeBase ( http://purl.org/phylo/treebase/phylows/study/TB2:S15832) and as Supporting Information.

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