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      Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae

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          Abstract

          Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genomic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families—genes directly mediating interactions with plant chemical defenses—underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many insect lineages are ancient (>150 million years ago (mya)), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across Scaptomyza, a genus nested within Drosophila that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several nonherbivorous species. Comparative genomic analyses revealed that herbivorous Scaptomyza has among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant-binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on living plants (bitter or electrophilic phytotoxins) or their ancestral diet (fermenting plant volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight gene candidates that have also been linked to other dietary transitions in Drosophila.

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          Most cited references153

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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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              MUSCLE: multiple sequence alignment with high accuracy and high throughput.

              We describe MUSCLE, a new computer program for creating multiple alignments of protein sequences. Elements of the algorithm include fast distance estimation using kmer counting, progressive alignment using a new profile function we call the log-expectation score, and refinement using tree-dependent restricted partitioning. The speed and accuracy of MUSCLE are compared with T-Coffee, MAFFT and CLUSTALW on four test sets of reference alignments: BAliBASE, SABmark, SMART and a new benchmark, PREFAB. MUSCLE achieves the highest, or joint highest, rank in accuracy on each of these sets. Without refinement, MUSCLE achieves average accuracy statistically indistinguishable from T-Coffee and MAFFT, and is the fastest of the tested methods for large numbers of sequences, aligning 5000 sequences of average length 350 in 7 min on a current desktop computer. The MUSCLE program, source code and PREFAB test data are freely available at http://www.drive5. com/muscle.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                G3 (Bethesda)
                Genetics
                g3journal
                G3: Genes|Genomes|Genetics
                Oxford University Press (US )
                2160-1836
                August 2023
                15 June 2023
                15 June 2023
                : 13
                : 8
                : jkad133
                Affiliations
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Biology, Brandeis University , Waltham, MA 02453, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                Department of Biology and Center for Genomics and Systems Biology, New York University , New York, NY 10003, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                Department of Biology, Stanford University , Palo Alto, CA 94305, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                National Center for Biotechnology Information , National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Biology, Stanford University , Palo Alto, CA 94305, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                Boyce Thompson Institute, Cornell University, Ithaca, NY 14853, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Chemistry & Biochemistry, University of Oregon , Eugene, OR 97403, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Biology, Stanford University , Palo Alto, CA 94305, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                Department of Biology and Center for Genomics and Systems Biology, New York University , New York, NY 10003, USA
                Department of Nematology, University of California Riverside , Riverside, CA 92521, USA
                Department of Botany and Plant Sciences, University of California Riverside , Riverside, CA 92521, USA
                Center for Plant Cell Biology and Institute for Integrative Genome Biology, University of California Riverside , Riverside, CA 92521, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                Department of Biology, University of Texas Permian Basin , Odessa, TX 79762, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Molecular Biology Institute, University of California Los Angeles , Los Angeles, CA 90095, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Biology, Stanford University , Palo Alto, CA 94305, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                Jacobs Institute, Cornell Tech , New York, NY 10044, USA
                FIND Genomics , New York, NY 10044, USA
                Department of Ecology and Evolutionary Biology, University of Arizona , Tucson, AZ 85721, USA
                Department of Botany and Plant Sciences, University of California Riverside , Riverside, CA 92521, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Biomedical Engineering, Viterbi School of Engineering, University of Southern California , Los Angeles, CA 90007, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Integrative Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Department of Molecular and Cell Biology, University of California Berkeley , Berkeley, CA 94720, USA
                Author notes
                Corresponding author: Carl J. Shapiro Science Center, Brandeis University, 2-16, Waltham, MA 02453, USA. Email: jpelaez@ 123456brandeis.edu ; *Corresponding author: University of California Berkeley, 142 Weill Hall #3200, Berkeley, CA 94720, USA. Email: whiteman@ 123456berkeley.edu

                Conflicts of interest statement The author(s) declare no conflict of interest.

                Author information
                https://orcid.org/0000-0003-1448-4678
                Article
                jkad133
                10.1093/g3journal/jkad133
                10411586
                37317982
                a67048e8-f071-405b-8fa2-bc8905cf57ad
                © The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 March 2023
                : 31 May 2023
                : 23 June 2023
                Page count
                Pages: 17
                Funding
                Funded by: National Science Foundation, DOI 10.13039/501100008982;
                Funded by: NSF, DOI 10.13039/100000001;
                Funded by: National Institutes of Health, DOI 10.13039/100000002;
                Funded by: United States Department of Agriculture, DOI 10.13039/100000199;
                Funded by: University of California, DOI 10.13039/100005595;
                Funded by: National Geographic Society, DOI 10.13039/100006363;
                Funded by: John Templeton Foundation, DOI 10.13039/100000925;
                Categories
                Investigation
                AcademicSubjects/SCI01180
                AcademicSubjects/SCI01140

                Genetics
                scaptomyza,gene family evolution,genomics,trophic shift,drosophila,plant-herbivore interactions,adaptation

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