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      A Large-Scale, Higher-Level, Molecular Phylogenetic Study of the Insect Order Lepidoptera (Moths and Butterflies)

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          Abstract

          Background

          Higher-level relationships within the Lepidoptera, and particularly within the species-rich subclade Ditrysia, are generally not well understood, although recent studies have yielded progress. We present the most comprehensive molecular analysis of lepidopteran phylogeny to date, focusing on relationships among superfamilies.

          Methodology / Principal Findings

          483 taxa spanning 115 of 124 families were sampled for 19 protein-coding nuclear genes, from which maximum likelihood tree estimates and bootstrap percentages were obtained using GARLI. Assessment of heuristic search effectiveness showed that better trees and higher bootstrap percentages probably remain to be discovered even after 1000 or more search replicates, but further search proved impractical even with grid computing. Other analyses explored the effects of sampling nonsynonymous change only versus partitioned and unpartitioned total nucleotide change; deletion of rogue taxa; and compositional heterogeneity. Relationships among the non-ditrysian lineages previously inferred from morphology were largely confirmed, plus some new ones, with strong support. Robust support was also found for divergences among non-apoditrysian lineages of Ditrysia, but only rarely so within Apoditrysia. Paraphyly for Tineoidea is strongly supported by analysis of nonsynonymous-only signal; conflicting, strong support for tineoid monophyly when synonymous signal was added back is shown to result from compositional heterogeneity.

          Conclusions / Significance

          Support for among-superfamily relationships outside the Apoditrysia is now generally strong. Comparable support is mostly lacking within Apoditrysia, but dramatically increased bootstrap percentages for some nodes after rogue taxon removal, and concordance with other evidence, strongly suggest that our picture of apoditrysian phylogeny is approximately correct. This study highlights the challenge of finding optimal topologies when analyzing hundreds of taxa. It also shows that some nodes get strong support only when analysis is restricted to nonsynonymous change, while total change is necessary for strong support of others. Thus, multiple types of analyses will be necessary to fully resolve lepidopteran phylogeny.

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          Most cited references20

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          Insect diversity in the fossil record.

          Insects possess a surprisingly extensive fossil record. Compilation of the geochronologic ranges of insect families demonstrates that their diversity exceeds that of preserved vertebrate tetrapods through 91 percent of their evolutionary history. The great diversity of insects was achieved not by high origination rates but rather by low extinction rates comparable to the low rates of slowly evolving marine invertebrate groups. The great radiation of modern insects began 245 million years ago and was not accelerated by the expansion of angiosperms during the Cretaceous period. The basic trophic machinery of insects was in place nearly 100 million years before angiosperms appeared in the fossil record.
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            Pruning Rogue Taxa Improves Phylogenetic Accuracy: An Efficient Algorithm and Webservice

            The presence of rogue taxa (rogues) in a set of trees can frequently have a negative impact on the results of a bootstrap analysis (e.g., the overall support in consensus trees). We introduce an efficient graph-based algorithm for rogue taxon identification as well as an interactive webservice implementing this algorithm. Compared with our previous method, the new algorithm is up to 4 orders of magnitude faster, while returning qualitatively identical results. Because of this significant improvement in scalability, the new algorithm can now identify substantially more complex and compute-intensive rogue taxon constellations. On a large and diverse collection of real-world data sets, we show that our method yields better supported reduced/pruned consensus trees than any competing rogue taxon identification method. Using the parallel version of our open-source code, we successfully identified rogue taxa in a set of 100 trees with 116 334 taxa each. For simulated data sets, we show that when removing/pruning rogue taxa with our method from a tree set, we consistently obtain bootstrap consensus trees as well as maximum-likelihood trees that are topologically closer to the respective true trees.
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              Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study

              Background In the mega-diverse insect order Lepidoptera (butterflies and moths; 165,000 described species), deeper relationships are little understood within the clade Ditrysia, to which 98% of the species belong. To begin addressing this problem, we tested the ability of five protein-coding nuclear genes (6.7 kb total), and character subsets therein, to resolve relationships among 123 species representing 27 (of 33) superfamilies and 55 (of 100) families of Ditrysia under maximum likelihood analysis. Results Our trees show broad concordance with previous morphological hypotheses of ditrysian phylogeny, although most relationships among superfamilies are weakly supported. There are also notable surprises, such as a consistently closer relationship of Pyraloidea than of butterflies to most Macrolepidoptera. Monophyly is significantly rejected by one or more character sets for the putative clades Macrolepidoptera as currently defined (P < 0.05) and Macrolepidoptera excluding Noctuoidea and Bombycoidea sensu lato (P ≤ 0.005), and nearly so for the superfamily Drepanoidea as currently defined (P < 0.08). Superfamilies are typically recovered or nearly so, but usually without strong support. Relationships within superfamilies and families, however, are often robustly resolved. We provide some of the first strong molecular evidence on deeper splits within Pyraloidea, Tortricoidea, Geometroidea, Noctuoidea and others. Separate analyses of mostly synonymous versus non-synonymous character sets revealed notable differences (though not strong conflict), including a marked influence of compositional heterogeneity on apparent signal in the third codon position (nt3). As available model partitioning methods cannot correct for this variation, we assessed overall phylogeny resolution through separate examination of trees from each character set. Exploration of "tree space" with GARLI, using grid computing, showed that hundreds of searches are typically needed to find the best-feasible phylogeny estimate for these data. Conclusion Our results (a) corroborate the broad outlines of the current working phylogenetic hypothesis for Ditrysia, (b) demonstrate that some prominent features of that hypothesis, including the position of the butterflies, need revision, and (c) resolve the majority of family and subfamily relationships within superfamilies as thus far sampled. Much further gene and taxon sampling will be needed, however, to strongly resolve individual deeper nodes.
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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
                2013
                12 March 2013
                21 March 2013
                : 8
                : 3
                Affiliations
                [1 ]Institute for Bioscience and Biotechnology Research, University of Maryland, College Park, Maryland, United States of America
                [2 ]Department of Entomology, University of Maryland, College Park, Maryland, United States of America
                [3 ]Entomology, State Museum of Natural History, Stuttgart, Germany
                [4 ]Laboratory of Molecular Evolution, Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland, United States of America
                [5 ]Florida Museum of Natural History, Gainesville, Florida, United States of America
                [6 ]Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, United States of America
                [7 ]Department of Plant Medicine, Chungbuk National University, Cheongju, Korea
                [8 ]Department of Entomology, Smithsonian Institution, Washington, District of Columbia, United States of America
                [9 ]Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain
                [10 ]Systematic Entomology Lab, Agricultural Research Service, United States Department of Agriculture, Beltsville, Maryland, United States of America
                [11 ]Encyclopedia of Life, Smithsonian Institution, Washington, District of Columbia, United States of America
                [12 ]Department of Entomology, University of Minnesota, Saint Paul, Minnesota, United States of America
                [13 ]Department of Life Sciences, Natural History Museum, London, England
                Field Museum of Natural History, United States of America
                Author notes

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

                Oversaw taxon collection: CM. Helped oversee taxon collection: KTM. Directed sequence generation: JCR. Assembled, error-checked, and submitted all sequences to GenBank: JCR AZ AYK. Conceived all analyses: JCR CM MPC AZ AYK ALB DJZ J-CS. Performed phylogenetic analyses: JCR AZ ALB J-CS. Wrote and assembled the manuscript: JCR CM. Commented on the manuscript: JCR CM MPC AZ AYK ALB DJZ J-CS SC DRD JB JB CP SW DCL KTM.

                Article
                PONE-D-12-40081
                10.1371/journal.pone.0058568
                3595289
                23554903
                7b2b01ee-8022-4585-860e-efdd8cff8a23

                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
                Pages: 23
                Funding
                Financial support was provided by the U. S. National Science Foundation‘s Assembling the Tree of Life program, award numbers 1042845, 0531626, and 0531769. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Computational Biology
                Evolutionary Modeling
                Evolutionary Biology
                Evolutionary Systematics
                Molecular Systematics
                Phylogenetics
                Taxonomy
                Organismal Evolution
                Animal Evolution
                Evolutionary Genetics
                Population Genetics
                Population Biology
                Population Genetics
                Zoology
                Animal Phylogenetics
                Animal Taxonomy

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