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      Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes

      research-article
      22 , , 13 , 16 , 6 , 2 , 24 , 13 , 15 , 21 , 6 , 24 , 33 , 5 , 24 , 19 , 10 , 16 , 30 , 6 , 27 , 12 , 29 , 23 , 12 , 6 , 11 , 25 , 13 , 7 , 20 , 17 , 32 , 2 , 14 , 8 , 29 , 13 , 34 , 16 , 18 , 24 , 8 , 29 , 15 , 29 , 1 , 31 , 32 , 28 , 11 , 35 , 9 , 32 , 36 , 26 , 4 , 35 , 32 , 3 , 35 ,
      Genome Biology
      BioMed Central
      Tsetse, Trypanosomiasis, Hematophagy, Lactation, Disease, Neglected, Symbiosis

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          Abstract

          Background

          Tsetse flies ( Glossina sp.) are the vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse flies are distinguished from other Diptera by unique adaptations, including lactation and the birthing of live young (obligate viviparity), a vertebrate blood-specific diet by both sexes, and obligate bacterial symbiosis. This work describes the comparative analysis of six Glossina genomes representing three sub-genera: Morsitans ( G. morsitans morsitans, G. pallidipes, G. austeni), Palpalis ( G. palpalis, G. fuscipes), and Fusca ( G. brevipalpis) which represent different habitats, host preferences, and vectorial capacity.

          Results

          Genomic analyses validate established evolutionary relationships and sub-genera. Syntenic analysis of Glossina relative to Drosophila melanogaster shows reduced structural conservation across the sex-linked X chromosome. Sex-linked scaffolds show increased rates of female-specific gene expression and lower evolutionary rates relative to autosome associated genes. Tsetse-specific genes are enriched in protease, odorant-binding, and helicase activities. Lactation-associated genes are conserved across all Glossina species while male seminal proteins are rapidly evolving. Olfactory and gustatory genes are reduced across the genus relative to other insects. Vision-associated Rhodopsin genes show conservation of motion detection/tracking functions and variance in the Rhodopsin detecting colors in the blue wavelength ranges.

          Conclusions

          Expanded genomic discoveries reveal the genetics underlying Glossina biology and provide a rich body of knowledge for basic science and disease control. They also provide insight into the evolutionary biology underlying novel adaptations and are relevant to applied aspects of vector control such as trap design and discovery of novel pest and disease control strategies.

          Electronic supplementary material

          The online version of this article (10.1186/s13059-019-1768-2) contains supplementary material, which is available to authorized users.

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          Most cited references110

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          tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence

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            TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations

            We present TranslatorX, a web server designed to align protein-coding nucleotide sequences based on their corresponding amino acid translations. Many comparisons between biological sequences (nucleic acids and proteins) involve the construction of multiple alignments. Alignments represent a statement regarding the homology between individual nucleotides or amino acids within homologous genes. As protein-coding DNA sequences evolve as triplets of nucleotides (codons) and it is known that sequence similarity degrades more rapidly at the DNA than at the amino acid level, alignments are generally more accurate when based on amino acids than on their corresponding nucleotides. TranslatorX novelties include: (i) use of all documented genetic codes and the possibility of assigning different genetic codes for each sequence; (ii) a battery of different multiple alignment programs; (iii) translation of ambiguous codons when possible; (iv) an innovative criterion to clean nucleotide alignments with GBlocks based on protein information; and (v) a rich output, including Jalview-powered graphical visualization of the alignments, codon-based alignments coloured according to the corresponding amino acids, measures of compositional bias and first, second and third codon position specific alignments. The TranslatorX server is freely available at http://translatorx.co.uk.
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              Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology.

              Datamonkey is a popular web-based suite of phylogenetic analysis tools for use in evolutionary biology. Since the original release in 2005, we have expanded the analysis options to include recently developed algorithmic methods for recombination detection, evolutionary fingerprinting of genes, codon model selection, co-evolution between sites, identification of sites, which rapidly escape host-immune pressure and HIV-1 subtype assignment. The traditional selection tools have also been augmented to include recent developments in the field. Here, we summarize the analyses options currently available on Datamonkey, and provide guidelines for their use in evolutionary biology. Availability and documentation: http://www.datamonkey.org.
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                Author and article information

                Contributors
                gmattardo@ucdavis.edu
                a.m.m.abd-alla@iaea.org
                alvaro.acosta-serrano@lstmed.ac.uk
                jallen@ebi.ac.uk
                batetarw@gmail.com
                joshua.benoit@uc.edu
                K.Bourtzis@iaea.org
                jellecrs@gmail.com
                Guy.Caljon@uantwerpen.be
                mikkel@ebi.ac.uk
                farrowdw@mail.uc.edu
                friedrichwsu@gmail.com
                aurelie.hua-van@egce.cnrs-gif.fr
                jenninec@mail.uc.edu
                dmlarkin@gmail.com
                daniel.lawson@imperial.ac.uk
                mike.lehane@lstmed.ac.uk
                vasilis.lenis@plymouth.ac.uk
                ernesto@ebi.ac.uk
                rwanjiru@icipe.org , rslnmacharia1@gmail.com
                malacrid@unipv.it
                heather.marco@uct.ac.za
                dmasiga@icipe.org
                gmaslen@ebi.ac.uk
                irina.matetovici@vib.be
                rpmeisel@uh.edu
                irene_meki@yahoo.com
                vmichalk@fiu.edu , vmichalkova@yahoo.com
                wolfgang.miller@meduniwien.ac.at
                pminx77@gmail.com
                mireji.paul@gmail.com
                lino.ometto@unipv.it
                a.g.parker@iaea.org
                Rita.Rio@mail.wvu.edu
                clair.rose@lstmed.ac.uk
                andrew.rosendale@msj.edu
                omar.rota@fmach.it
                grazia.savini01@universitadipavia.it
                liliane.schoofs@kuleuven.be
                francesca.scolari@unipv.it
                mts11@aber.ac.uk
                peter.takac@savba.sk , Peter@scientica.sk
                ctomlins@wustl.edu
                gtsiamis1@gmail.com
                jvdabbeele@itg.be
                aurelien.vigneron@yale.edu
                jingwenwang@fudan.edu.cn
                warrenwc@missouri.edu
                robert.waterhouse@unil.ch
                matthew.weirauch@cchmc.org
                brian.weiss@yale.edu
                rwilson@genome.wustl.edu
                kitty.zhaoxin@foxmail.com
                serap.aksoy@yale.edu
                Journal
                Genome Biol
                Genome Biol
                Genome Biology
                BioMed Central (London )
                1474-7596
                1474-760X
                2 September 2019
                2 September 2019
                2019
                : 20
                : 187
                Affiliations
                [1 ]ISNI 0000000121682483, GRID grid.8186.7, Institute of Biological, Environmental and Rural Sciences, , Aberystwyth University, ; Aberystwyth, Ceredigion UK
                [2 ]GRID grid.473294.f, Department of Biochemistry, , Biotechnology Research Institute - Kenya Agricultural and Livestock Research Organization, ; Kikuyu, Kenya
                [3 ]ISNI 0000000119573309, GRID grid.9227.e, CAS Center for Influenza Research and Early-warning (CASCIRE), , Chinese Academy of Sciences, ; Beijing, China
                [4 ]ISNI 0000 0000 9025 8099, GRID grid.239573.9, Center for Autoimmune Genomics and Etiology and Divisions of Biomedical Informatics and Developmental Biology, , Cincinnati Children’s Hospital Medical Center, ; Cincinnati, OH USA
                [5 ]ISNI 0000 0004 4910 6535, GRID grid.460789.4, Laboratoire Evolution, Genomes, Comportement, Ecologie, CNRS, IRD, , Univ. Paris-Sud, Université Paris-Saclay, ; Gif-sur-Yvette, France
                [6 ]ISNI 0000 0000 9709 7726, GRID grid.225360.0, VectorBase, European Molecular Biology Laboratory, , European Bioinformatics Institute (EMBL-EBI), ; Cambridge, Cambridgeshire UK
                [7 ]ISNI 0000 0001 2110 1845, GRID grid.65456.34, Department of Biological Sciences, , Florida International University, ; Miami, Florida USA
                [8 ]ISNI 0000 0004 1755 6224, GRID grid.424414.3, Department of Sustainable Ecosystems and Bioresources, Research and Innovation Centre, , Fondazione Edmund Mach, ; San Michele all’Adige, TN Italy
                [9 ]ISNI 0000 0001 0125 2443, GRID grid.8547.e, School of Life Sciences, , Fudan University, ; Shanghai, China
                [10 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Department of Life Sciences, , Imperial College London, ; London, UK
                [11 ]ISNI 0000 0001 2153 5088, GRID grid.11505.30, Biomedical Sciences, , Institute of Tropical Medicine, ; Antwerp, Belgium
                [12 ]ISNI 0000 0004 1794 5158, GRID grid.419326.b, Molecular Biology and Bioinformatics Unit, , International Center for Insect Physiology and Ecology, ; Nairobi, Kenya
                [13 ]ISNI 0000 0004 0403 8399, GRID grid.420221.7, Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & Agriculture, ; Vienna, Vienna Austria
                [14 ]ISNI 0000 0001 0155 5938, GRID grid.33058.3d, Centre for Geographic Medicine Research Coast, , Kenya Medical Research Institute, ; Kilifi, Kenya
                [15 ]ISNI 0000 0001 0668 7884, GRID grid.5596.f, Department of Biology - Functional Genomics and Proteomics Group, , KU Leuven, ; Leuven, Belgium
                [16 ]ISNI 0000 0004 1936 9764, GRID grid.48004.38, Department of Vector Biology, , Liverpool School of Tropical Medicine, ; Merseyside, Liverpool UK
                [17 ]ISNI 0000 0000 9259 8492, GRID grid.22937.3d, Department of Cell and Developmental Biology, , Medical University of Vienna, ; Vienna, Austria
                [18 ]ISNI 0000 0000 8822 6207, GRID grid.418794.7, Department of Biology, , Mount St. Joseph University, ; Cincinnati, OH USA
                [19 ]ISNI 0000 0004 0425 573X, GRID grid.20931.39, Department of Comparative Biomedical Sciences, , Royal Veterinary College, ; London, UK
                [20 ]ISNI 0000 0001 2180 9405, GRID grid.419303.c, Institute of Zoology, , Slovak Academy of Sciences, ; Bratislava, Slovakia
                [21 ]ISNI 0000 0001 0790 3681, GRID grid.5284.b, Laboratory of Microbiology, Parasitology and Hygiene, , University of Antwerp, ; Antwerp, Belgium
                [22 ]ISNI 0000 0004 1936 9684, GRID grid.27860.3b, Department of Entomology and Nematology, , University of California, Davis, ; Davis, CA USA
                [23 ]ISNI 0000 0004 1937 1151, GRID grid.7836.a, Department of Biological Sciences, , University of Cape Town, ; Rondebosch, South Africa
                [24 ]ISNI 0000 0001 2179 9593, GRID grid.24827.3b, Department of Biological Sciences, , University of Cincinnati, ; Cincinnati, OH USA
                [25 ]ISNI 0000 0004 1569 9707, GRID grid.266436.3, Department of Biology and Biochemistry, , University of Houston, ; Houston, TX USA
                [26 ]ISNI 0000 0001 2165 4204, GRID grid.9851.5, Department of Ecology & Evolution, Swiss Institute of Bioinformatics, , University of Lausanne, ; Lausanne, Switzerland
                [27 ]ISNI 0000 0001 2019 0495, GRID grid.10604.33, Centre for Biotechnology and Bioinformatics, , University of Nairobi, ; Nairobi, Kenya
                [28 ]ISNI 0000 0004 0576 5395, GRID grid.11047.33, Department of Environmental and Natural Resources Management, , University of Patras, ; Agrinio, Etoloakarnania Greece
                [29 ]ISNI 0000 0004 1762 5736, GRID grid.8982.b, Department of Biology and Biotechnology, , University of Pavia, ; Pavia, Italy
                [30 ]ISNI 0000 0001 2219 0747, GRID grid.11201.33, Schools of Medicine and Dentistry, , University of Plymouth, ; Plymouth, UK
                [31 ]GRID grid.455086.a, Department of Animal Systematics, , Ústav zoológie SAV; Scientica, Ltd, ; Bratislava, Slovakia
                [32 ]ISNI 0000 0001 2355 7002, GRID grid.4367.6, McDonnell Genome Institute, , Washington University School of Medicine, ; St. Louis, MO USA
                [33 ]ISNI 0000 0001 1456 7807, GRID grid.254444.7, Department of Biological Sciences, , Wayne State University, ; Detroit, MI USA
                [34 ]ISNI 0000 0001 2156 6140, GRID grid.268154.c, Department of Biology, , West Virginia University, ; Morgantown, WV USA
                [35 ]ISNI 0000000419368710, GRID grid.47100.32, Department of Epidemiology of Microbial Diseases, , Yale School of Public Health, ; New Haven, CT USA
                [36 ]ISNI 0000 0001 2162 3504, GRID grid.134936.a, Bond Life Sciences Center, , University of Missouri, ; Columbia, MO USA
                Author information
                http://orcid.org/0000-0001-9941-143X
                Article
                1768
                10.1186/s13059-019-1768-2
                6721284
                31477173
                00453423-13f8-4a54-af21-99f4382f5856
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

                History
                : 31 January 2019
                : 22 July 2019
                Funding
                Funded by: National Institutes of Health (US)
                Award ID: D43 TW007391
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: U01AI115648
                Award ID: R01AI051584
                Award ID: R03TW008413
                Award ID: R03TW009444
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000060, National Institute of Allergy and Infectious Diseases;
                Award ID: R21AI109263
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000051, National Human Genome Research Institute;
                Award ID: U54HG003079
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100011512, National Research Foundation;
                Award ID: Grant # 10924
                Award Recipient :
                Funded by: Swiss National Science Foundation
                Award ID: PP00P3_170664
                Award Recipient :
                Funded by: Slovak Research and Development Agency
                Award ID: APVV-15-0604
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;
                Award ID: OPP1139763
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Genetics
                tsetse,trypanosomiasis,hematophagy,lactation,disease,neglected,symbiosis
                Genetics
                tsetse, trypanosomiasis, hematophagy, lactation, disease, neglected, symbiosis

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