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      Beyond Drosophila: resolving the rapid radiation of schizophoran flies with phylotranscriptomics

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          Abstract

          Background

          The most species-rich radiation of animal life in the 66 million years following the Cretaceous extinction event is that of schizophoran flies: a third of fly diversity including Drosophila fruit fly model organisms, house flies, forensic blow flies, agricultural pest flies, and many other well and poorly known true flies. Rapid diversification has hindered previous attempts to elucidate the phylogenetic relationships among major schizophoran clades. A robust phylogenetic hypothesis for the major lineages containing these 55,000 described species would be critical to understand the processes that contributed to the diversity of these flies. We use protein encoding sequence data from transcriptomes, including 3145 genes from 70 species, representing all superfamilies, to improve the resolution of this previously intractable phylogenetic challenge.

          Results

          Our results support a paraphyletic acalyptrate grade including a monophyletic Calyptratae and the monophyly of half of the acalyptrate superfamilies. The primary branching framework of Schizophora is well supported for the first time, revealing the primarily parasitic Pipunculidae and Sciomyzoidea stat. rev. as successive sister groups to the remaining Schizophora. Ephydroidea, Drosophila’s superfamily, is the sister group of Calyptratae. Sphaeroceroidea has modest support as the sister to all non-sciomyzoid Schizophora. We define two novel lineages corroborated by morphological traits, the ‘Modified Oviscapt Clade’ containing Tephritoidea, Nerioidea, and other families, and the ‘Cleft Pedicel Clade’ containing Calyptratae, Ephydroidea, and other families. Support values remain low among a challenging subset of lineages, including Diopsidae. The placement of these families remained uncertain in both concatenated maximum likelihood and multispecies coalescent approaches. Rogue taxon removal was effective in increasing support values compared with strategies that maximise gene coverage or minimise missing data.

          Conclusions

          Dividing most acalyptrate fly groups into four major lineages is supported consistently across analyses. Understanding the fundamental branching patterns of schizophoran flies provides a foundation for future comparative research on the genetics, ecology, and biocontrol.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12915-020-00944-8.

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          Trimmomatic: a flexible trimmer for Illumina sequence data

          Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.
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            MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

            We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.
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              RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

              Motivation: Phylogenies are increasingly used in all fields of medical and biological research. Moreover, because of the next-generation sequencing revolution, datasets used for conducting phylogenetic analyses grow at an unprecedented pace. RAxML (Randomized Axelerated Maximum Likelihood) is a popular program for phylogenetic analyses of large datasets under maximum likelihood. Since the last RAxML paper in 2006, it has been continuously maintained and extended to accommodate the increasingly growing input datasets and to serve the needs of the user community. Results: I present some of the most notable new features and extensions of RAxML, such as a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting post-analyses on sets of trees. In addition, an up-to-date 50-page user manual covering all new RAxML options is available. Availability and implementation: The code is available under GNU GPL at https://github.com/stamatak/standard-RAxML. Contact: alexandros.stamatakis@h-its.org Supplementary information: Supplementary data are available at Bioinformatics online.
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                Author and article information

                Contributors
                keith.bayless@csiro.au
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                8 February 2021
                8 February 2021
                2021
                : 19
                : 23
                Affiliations
                [1 ]GRID grid.1016.6, ISNI 0000 0001 2173 2719, Australian National Insect Collection, CSIRO National Research Collections Australia (NRCA), ; Acton, Canberra, ACT Australia
                [2 ]GRID grid.242287.9, ISNI 0000 0004 0461 6769, Department of Entomology, , California Academy of Sciences, ; San Francisco, CA USA
                [3 ]GRID grid.40803.3f, ISNI 0000 0001 2173 6074, Department of Entomology & Plant Pathology, , North Carolina State University, ; Raleigh, NC USA
                [4 ]GRID grid.452935.c, ISNI 0000 0001 2216 5875, Centre for Molecular Biodiversity Research (ZMB), , Zoologisches Forschungsmuseum Alexander Koenig (ZFMK), ; Bonn, Germany
                [5 ]GRID grid.5963.9, Department of Evolutionary Biology & Ecology, Institute of Biology I, , Albert Ludwig University of Freiburg, ; Hauptstraße 1, Freiburg i. Br., Germany
                [6 ]GRID grid.31501.36, ISNI 0000 0004 0470 5905, School of Biological Sciences, , Seoul National University, ; Seoul, Republic of Korea
                [7 ]GRID grid.4372.2, ISNI 0000 0001 2105 1091, Max-Planck-Institut of Immunobiology and Epigenetics, ; Freiburg, Germany
                [8 ]GRID grid.452935.c, ISNI 0000 0001 2216 5875, Centre of Taxonomy and Evolutionary Research, Arthropoda Department, , Zoological Research Museum Alexander Koenig, ; Bonn, Germany
                [9 ]GRID grid.4280.e, ISNI 0000 0001 2180 6431, Department of Biological Sciences, , National University of Singapore, ; Singapore, Singapore
                [10 ]GRID grid.4280.e, ISNI 0000 0001 2180 6431, Lee Kong Chian Natural History Museum, , National University of Singapore, ; Singapore, Singapore
                [11 ]GRID grid.4280.e, ISNI 0000 0001 2180 6431, Tropical Marine Science Institute, , National University of Singapore, ; Singapore, Singapore
                [12 ]GRID grid.22935.3f, ISNI 0000 0004 0530 8290, Department of Entomology, , China Agricultural University, ; Beijing, People’s Republic of China
                [13 ]GRID grid.452935.c, ISNI 0000 0001 2216 5875, Zoological Research Museum Alexander Koenig (ZFMK), ; Bonn, Germany
                Author information
                http://orcid.org/0000-0002-8283-7052
                Article
                944
                10.1186/s12915-020-00944-8
                7871583
                33407428
                64fd6009-c593-4cb2-bcb4-8d6b4080b4ba
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 20 May 2020
                : 17 December 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000155, Division of Environmental Biology;
                Award ID: DEB-1257960
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2021

                Life sciences
                diptera,phylogenomics,transcriptomes,drosophilidae,tephritidae
                Life sciences
                diptera, phylogenomics, transcriptomes, drosophilidae, tephritidae

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