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

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-spe...

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Main Authors: Geoffrey M. Attardo, Adly M. M. Abd-Alla, Alvaro Acosta-Serrano, James E. Allen, Rosemary Bateta, Joshua B. Benoit, Kostas Bourtzis, Jelle Caers, Guy Caljon, Mikkel B. Christensen, David W. Farrow, Markus Friedrich, Aurélie Hua-Van, Emily C. Jennings, Denis M. Larkin, Daniel Lawson, Michael J. Lehane, Vasileios P. Lenis, Ernesto Lowy-Gallego, Rosaline W. Macharia, Anna R. Malacrida, Heather G. Marco, Daniel Masiga, Gareth L. Maslen, Irina Matetovici, Richard P. Meisel, Irene Meki, Veronika Michalkova, Wolfgang J. Miller, Patrick Minx, Paul O. Mireji, Lino Ometto, Andrew G. Parker, Rita Rio, Clair Rose, Andrew J. Rosendale, Omar Rota-Stabelli, Grazia Savini, Liliane Schoofs, Francesca Scolari, Martin T. Swain, Peter Takáč, Chad Tomlinson, George Tsiamis, Jan Van Den Abbeele, Aurelien Vigneron, Jingwen Wang, Wesley C. Warren, Robert M. Waterhouse, Matthew T. Weirauch, Brian L. Weiss, Richard K. Wilson, Xin Zhao, Serap Aksoy
Format: Article
Language:English
Published: BMC 2019-09-01
Series:Genome Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13059-019-1768-2
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language English
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author Geoffrey M. Attardo
Adly M. M. Abd-Alla
Alvaro Acosta-Serrano
James E. Allen
Rosemary Bateta
Joshua B. Benoit
Kostas Bourtzis
Jelle Caers
Guy Caljon
Mikkel B. Christensen
David W. Farrow
Markus Friedrich
Aurélie Hua-Van
Emily C. Jennings
Denis M. Larkin
Daniel Lawson
Michael J. Lehane
Vasileios P. Lenis
Ernesto Lowy-Gallego
Rosaline W. Macharia
Anna R. Malacrida
Heather G. Marco
Daniel Masiga
Gareth L. Maslen
Irina Matetovici
Richard P. Meisel
Irene Meki
Veronika Michalkova
Wolfgang J. Miller
Patrick Minx
Paul O. Mireji
Lino Ometto
Andrew G. Parker
Rita Rio
Clair Rose
Andrew J. Rosendale
Omar Rota-Stabelli
Grazia Savini
Liliane Schoofs
Francesca Scolari
Martin T. Swain
Peter Takáč
Chad Tomlinson
George Tsiamis
Jan Van Den Abbeele
Aurelien Vigneron
Jingwen Wang
Wesley C. Warren
Robert M. Waterhouse
Matthew T. Weirauch
Brian L. Weiss
Richard K. Wilson
Xin Zhao
Serap Aksoy
spellingShingle Geoffrey M. Attardo
Adly M. M. Abd-Alla
Alvaro Acosta-Serrano
James E. Allen
Rosemary Bateta
Joshua B. Benoit
Kostas Bourtzis
Jelle Caers
Guy Caljon
Mikkel B. Christensen
David W. Farrow
Markus Friedrich
Aurélie Hua-Van
Emily C. Jennings
Denis M. Larkin
Daniel Lawson
Michael J. Lehane
Vasileios P. Lenis
Ernesto Lowy-Gallego
Rosaline W. Macharia
Anna R. Malacrida
Heather G. Marco
Daniel Masiga
Gareth L. Maslen
Irina Matetovici
Richard P. Meisel
Irene Meki
Veronika Michalkova
Wolfgang J. Miller
Patrick Minx
Paul O. Mireji
Lino Ometto
Andrew G. Parker
Rita Rio
Clair Rose
Andrew J. Rosendale
Omar Rota-Stabelli
Grazia Savini
Liliane Schoofs
Francesca Scolari
Martin T. Swain
Peter Takáč
Chad Tomlinson
George Tsiamis
Jan Van Den Abbeele
Aurelien Vigneron
Jingwen Wang
Wesley C. Warren
Robert M. Waterhouse
Matthew T. Weirauch
Brian L. Weiss
Richard K. Wilson
Xin Zhao
Serap Aksoy
Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes
Genome Biology
Tsetse
Trypanosomiasis
Hematophagy
Lactation
Disease
Neglected
author_facet Geoffrey M. Attardo
Adly M. M. Abd-Alla
Alvaro Acosta-Serrano
James E. Allen
Rosemary Bateta
Joshua B. Benoit
Kostas Bourtzis
Jelle Caers
Guy Caljon
Mikkel B. Christensen
David W. Farrow
Markus Friedrich
Aurélie Hua-Van
Emily C. Jennings
Denis M. Larkin
Daniel Lawson
Michael J. Lehane
Vasileios P. Lenis
Ernesto Lowy-Gallego
Rosaline W. Macharia
Anna R. Malacrida
Heather G. Marco
Daniel Masiga
Gareth L. Maslen
Irina Matetovici
Richard P. Meisel
Irene Meki
Veronika Michalkova
Wolfgang J. Miller
Patrick Minx
Paul O. Mireji
Lino Ometto
Andrew G. Parker
Rita Rio
Clair Rose
Andrew J. Rosendale
Omar Rota-Stabelli
Grazia Savini
Liliane Schoofs
Francesca Scolari
Martin T. Swain
Peter Takáč
Chad Tomlinson
George Tsiamis
Jan Van Den Abbeele
Aurelien Vigneron
Jingwen Wang
Wesley C. Warren
Robert M. Waterhouse
Matthew T. Weirauch
Brian L. Weiss
Richard K. Wilson
Xin Zhao
Serap Aksoy
author_sort Geoffrey M. Attardo
title Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes
title_short Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes
title_full Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes
title_fullStr Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes
title_full_unstemmed Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes
title_sort comparative genomic analysis of six glossina genomes, vectors of african trypanosomes
publisher BMC
series Genome Biology
issn 1474-760X
publishDate 2019-09-01
description 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.
topic Tsetse
Trypanosomiasis
Hematophagy
Lactation
Disease
Neglected
url http://link.springer.com/article/10.1186/s13059-019-1768-2
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spelling doaj-cc3ed49129c9474f93f589276ff7bcfe2020-11-25T03:44:59ZengBMCGenome Biology1474-760X2019-09-0120113110.1186/s13059-019-1768-2Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomesGeoffrey M. Attardo0Adly M. M. Abd-Alla1Alvaro Acosta-Serrano2James E. Allen3Rosemary Bateta4Joshua B. Benoit5Kostas Bourtzis6Jelle Caers7Guy Caljon8Mikkel B. Christensen9David W. Farrow10Markus Friedrich11Aurélie Hua-Van12Emily C. Jennings13Denis M. Larkin14Daniel Lawson15Michael J. Lehane16Vasileios P. Lenis17Ernesto Lowy-Gallego18Rosaline W. Macharia19Anna R. Malacrida20Heather G. Marco21Daniel Masiga22Gareth L. Maslen23Irina Matetovici24Richard P. Meisel25Irene Meki26Veronika Michalkova27Wolfgang J. Miller28Patrick Minx29Paul O. Mireji30Lino Ometto31Andrew G. Parker32Rita Rio33Clair Rose34Andrew J. Rosendale35Omar Rota-Stabelli36Grazia Savini37Liliane Schoofs38Francesca Scolari39Martin T. Swain40Peter Takáč41Chad Tomlinson42George Tsiamis43Jan Van Den Abbeele44Aurelien Vigneron45Jingwen Wang46Wesley C. Warren47Robert M. Waterhouse48Matthew T. Weirauch49Brian L. Weiss50Richard K. Wilson51Xin Zhao52Serap Aksoy53Department of Entomology and Nematology, University of California, DavisInsect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & AgricultureDepartment of Vector Biology, Liverpool School of Tropical MedicineVectorBase, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI)Department of Biochemistry, Biotechnology Research Institute - Kenya Agricultural and Livestock Research OrganizationDepartment of Biological Sciences, University of CincinnatiInsect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & AgricultureDepartment of Biology - Functional Genomics and Proteomics Group, KU LeuvenLaboratory of Microbiology, Parasitology and Hygiene, University of AntwerpVectorBase, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI)Department of Biological Sciences, University of CincinnatiDepartment of Biological Sciences, Wayne State UniversityLaboratoire Evolution, Genomes, Comportement, Ecologie, CNRS, IRD, Univ. Paris-Sud, Université Paris-SaclayDepartment of Biological Sciences, University of CincinnatiDepartment of Comparative Biomedical Sciences, Royal Veterinary CollegeDepartment of Life Sciences, Imperial College LondonDepartment of Vector Biology, Liverpool School of Tropical MedicineSchools of Medicine and Dentistry, University of PlymouthVectorBase, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI)Molecular Biology and Bioinformatics Unit, International Center for Insect Physiology and EcologyDepartment of Biology and Biotechnology, University of PaviaDepartment of Biological Sciences, University of Cape TownMolecular Biology and Bioinformatics Unit, International Center for Insect Physiology and EcologyVectorBase, European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI)Biomedical Sciences, Institute of Tropical MedicineDepartment of Biology and Biochemistry, University of HoustonInsect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & AgricultureDepartment of Biological Sciences, Florida International UniversityDepartment of Cell and Developmental Biology, Medical University of ViennaMcDonnell Genome Institute, Washington University School of MedicineDepartment of Biochemistry, Biotechnology Research Institute - Kenya Agricultural and Livestock Research OrganizationDepartment of Sustainable Ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund MachInsect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food & AgricultureDepartment of Biology, West Virginia UniversityDepartment of Vector Biology, Liverpool School of Tropical MedicineDepartment of Biology, Mount St. Joseph UniversityDepartment of Sustainable Ecosystems and Bioresources, Research and Innovation Centre, Fondazione Edmund MachDepartment of Biology and Biotechnology, University of PaviaDepartment of Biology - Functional Genomics and Proteomics Group, KU LeuvenDepartment of Biology and Biotechnology, University of PaviaInstitute of Biological, Environmental and Rural Sciences, Aberystwyth UniversityDepartment of Animal Systematics, Ústav zoológie SAV; Scientica, LtdMcDonnell Genome Institute, Washington University School of MedicineDepartment of Environmental and Natural Resources Management, University of PatrasBiomedical Sciences, Institute of Tropical MedicineDepartment of Epidemiology of Microbial Diseases, Yale School of Public HealthSchool of Life Sciences, Fudan UniversityMcDonnell Genome Institute, Washington University School of MedicineDepartment of Ecology & Evolution, Swiss Institute of Bioinformatics, University of LausanneCenter for Autoimmune Genomics and Etiology and Divisions of Biomedical Informatics and Developmental Biology, Cincinnati Children’s Hospital Medical CenterDepartment of Epidemiology of Microbial Diseases, Yale School of Public HealthMcDonnell Genome Institute, Washington University School of MedicineCAS Center for Influenza Research and Early-warning (CASCIRE), Chinese Academy of SciencesDepartment of Epidemiology of Microbial Diseases, Yale School of Public HealthAbstract 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.http://link.springer.com/article/10.1186/s13059-019-1768-2TsetseTrypanosomiasisHematophagyLactationDiseaseNeglected