Gene content evolution in the arthropods.

Arthropods DNA methylation Evolution Gene content Genome assembly Genomics Protein domains

Journal

Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660

Informations de publication

Date de publication:
23 01 2020
Historique:
received: 06 11 2019
accepted: 26 12 2019
entrez: 24 1 2020
pubmed: 24 1 2020
medline: 5 1 2021
Statut: epublish

Résumé

Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception. These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

Sections du résumé

BACKGROUND
Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods.
RESULTS
Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality, and chemoperception.
CONCLUSIONS
These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.

Identifiants

pubmed: 31969194
doi: 10.1186/s13059-019-1925-7
pii: 10.1186/s13059-019-1925-7
pmc: PMC6977273
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

15

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM070559
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI131427
Pays : United States
Organisme : NHGRI NIH HHS
ID : U54 HG003273
Pays : United States

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Auteurs

Gregg W C Thomas (GWC)

Department of Biology and Department of Computer Science, Indiana University, Bloomington, IN, USA.

Elias Dohmen (E)

Institute for Evolution and Biodiversity, University of Münsterss, 48149, Münster, Germany.
Institute for Bioinformatics and Chemoinformatics, University of Hamburg, Hamburg, Germany.
Westphalian University of Applied Sciences, 45665, Recklinghausen, Germany.

Daniel S T Hughes (DST)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Present Address: Institute for Genomic Medicine, Columbia University, New York, NY, 10032, USA.

Shwetha C Murali (SC)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Present Address: Howard Hughes Medical Institute, Department of Genome Sciences, University of Washington, Seattle, WA, 98195, USA.

Monica Poelchau (M)

National Agricultural Library, USDA, Beltsville, MD, 20705, USA.

Karl Glastad (K)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.
Present Address: Penn Epigenetics Institute, Department of Cell and Developmental Biology, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, 19104, USA.

Clare A Anstead (CA)

Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, 3010, Australia.

Nadia A Ayoub (NA)

Department of Biology, Washington and Lee University, 204 West Washington Street, Lexington, VA, 24450, USA.

Phillip Batterham (P)

School of BioSciences Science Faculty, The University of Melbourne, Melbourne, VIC, 3010, Australia.

Michelle Bellair (M)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.
Present Address: CooperGenomics, Houston, TX, USA.

Greta J Binford (GJ)

Department of Biology, Lewis & Clark College, Portland, OR, 97219, USA.

Hsu Chao (H)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Yolanda H Chen (YH)

Department of Plant and Soil Sciences, University of Vermont, Burlington, USA.

Christopher Childers (C)

National Agricultural Library, USDA, Beltsville, MD, 20705, USA.

Huyen Dinh (H)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Harsha Vardhan Doddapaneni (HV)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Jian J Duan (JJ)

Beneficial Insects Introduction Research Unit, United States Department of Agriculture, Agricultural Research Service, Newark, DE, USA.

Shannon Dugan (S)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Lauren A Esposito (LA)

Institute for Biodiversity Science and Sustainability, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA, 94118, USA.

Markus Friedrich (M)

Department of Biological Sciences, Wayne State University, Detroit, MI, 48202, USA.

Jessica Garb (J)

Department of Biological Sciences, University of Massachusetts Lowell, 198 Riverside Street, Lowell, MA, 01854, USA.

Robin B Gasser (RB)

Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, 3010, Australia.

Michael A D Goodisman (MAD)

School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, 30332, USA.

Dawn E Gundersen-Rindal (DE)

USDA-ARS Invasive Insect Biocontrol and Behavior Laboratory, Beltsville, MD, USA.

Yi Han (Y)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Alfred M Handler (AM)

USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology, 1700 S.W. 23rd Drive, Gainesville, FL, 32608, USA.

Masatsugu Hatakeyama (M)

Division of Insect Sciences, National Institute of Agrobiological Sciences, Owashi, Tsukuba, 305-8634, Japan.

Lars Hering (L)

Department of Zoology, Institute of Biology, University of Kassel, 34132, Kassel, Germany.

Wayne B Hunter (WB)

USDA ARS, U. S. Horticultural Research Laboratory, Ft. Pierce, FL, 34945, USA.

Panagiotis Ioannidis (P)

Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.
Present Address: Foundation for Research and Technology Hellas, Institute of Molecular Biology and Biotechnology, Vassilika Vouton, 70013, Heraklion, Greece.

Joy C Jayaseelan (JC)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Divya Kalra (D)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Abderrahman Khila (A)

Université de Lyon, Institut de Génomique Fonctionnelle de Lyon, CNRS UMR 5242, Ecole Normale Supérieure de Lyon, Université Claude Bernard Lyon 1, 46 allée d'Italie, 69364, Lyon, France.

Pasi K Korhonen (PK)

Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, 3010, Australia.

Carol Eunmi Lee (CE)

Department of Integrative Biology, University of Wisconsin, Madison, WI, 53706, USA.

Sandra L Lee (SL)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Yiyuan Li (Y)

Department of Biological Sciences, University of Notre Dame, 109B Galvin Life Sciences, Notre Dame, IN, 46556, USA.

Amelia R I Lindsey (ARI)

Department of Entomology, University of California Riverside, Riverside, CA, USA.
Present Address: Department of Biology, Indiana University, Bloomington, IN, USA.

Georg Mayer (G)

Department of Zoology, Institute of Biology, University of Kassel, 34132, Kassel, Germany.

Alistair P McGregor (AP)

Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK.

Duane D McKenna (DD)

Department of Biological Sciences, University of Memphis, 3700 Walker Ave, Memphis, TN, 38152, USA.

Bernhard Misof (B)

Center for Molecular Biodiversity Research, Zoological Research Museum Alexander Koenig, Bonn, Germany.

Mala Munidasa (M)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Monica Munoz-Torres (M)

Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, USA.
Present Address: Phoenix Bioinformatics, 39221 Paseo Padre Parkway, Ste. J., Fremont, CA, 94538, USA.

Donna M Muzny (DM)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Oliver Niehuis (O)

Evolutionary Biology and Ecology, Institute of Biology I (Zoology), Albert Ludwig University of Freiburg, 79104, Freiburg (Brsg.), Germany.

Nkechinyere Osuji-Lacy (N)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Subba R Palli (SR)

Department of Entomology, University of Kentucky, Lexington, KY, 40546, USA.

Kristen A Panfilio (KA)

School of Life Sciences, University of Warwick, Gibbet Hill Campus, Coventry, CV4 7AL, UK.

Matthias Pechmann (M)

Cologne Biocenter, Zoological Institute, Department of Developmental Biology, University of Cologne, 50674, Cologne, Germany.

Trent Perry (T)

School of BioSciences Science Faculty, The University of Melbourne, Melbourne, VIC, 3010, Australia.

Ralph S Peters (RS)

Centre of Taxonomy and Evolutionary Research, Arthropoda Department, Zoological Research Museum Alexander Koenig, Bonn, Germany.

Helen C Poynton (HC)

School for the Environment, University of Massachusetts Boston, Boston, MA, 02125, USA.

Nikola-Michael Prpic (NM)

Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Abteilung für Entwicklungsbiologie, Georg-August-Universität Göttingen, Göttingen, Germany.
Göttingen Center for Molecular Biosciences (GZMB), Georg-August-Universität Göttingen, Göttingen, Germany.

Jiaxin Qu (J)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Dorith Rotenberg (D)

Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, 27606, USA.

Coby Schal (C)

Department of Entomology and W.M. Keck Center for Behavioral Biology, North Carolina State University, Raleigh, NC, 27695, USA.

Sean D Schoville (SD)

Department of Entomology, University of Wisconsin-Madison, Madison, USA.

Erin D Scully (ED)

Stored Product Insect and Engineering Research Unit, USDA-ARS Center for Grain and Animal Health Research, Manhattan, KS, 66502, USA.

Evette Skinner (E)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Daniel B Sloan (DB)

Department of Biology, Colorado State University, Ft. Collins, CO, USA.

Richard Stouthamer (R)

Department of Entomology, University of California Riverside, Riverside, CA, USA.

Michael R Strand (MR)

Department of Entomology, University of Georgia, Athens, GA, USA.

Nikolaus U Szucsich (NU)

Present Address: Arkansas Biosciences Institute, Arkansas State University, Jonesboro, AR, USA.

Asela Wijeratne (A)

Department of Biological Sciences, University of Memphis, 3700 Walker Ave, Memphis, TN, 38152, USA.
Natural History Museum Vienna, Burgring 7, 1010, Vienna, Austria.

Neil D Young (ND)

Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, VIC, 3010, Australia.

Eduardo E Zattara (EE)

INIBIOMA, Univ. Nacional del Comahue - CONICET, Bariloche, Argentina.

Joshua B Benoit (JB)

Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA.

Evgeny M Zdobnov (EM)

Department of Genetic Medicine and Development and Swiss Institute of Bioinformatics, University of Geneva, 1211, Geneva, Switzerland.

Michael E Pfrender (ME)

Department of Biological Sciences, University of Notre Dame, 109B Galvin Life Sciences, Notre Dame, IN, 46556, USA.

Kevin J Hackett (KJ)

Crop Production and Protection, U.S. Department of Agriculture-Agricultural Research Service, Beltsville, MD, 20705, USA.

John H Werren (JH)

Department of Biology, University of Rochester, Rochester, NY, 14627, USA.

Kim C Worley (KC)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Richard A Gibbs (RA)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA.

Ariel D Chipman (AD)

Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Givat Ram, 91904, Jerusalem, Israel.

Robert M Waterhouse (RM)

Department of Ecology & Evolution and Swiss Institute of Bioinformatics, University of Lausanne, 1015, Lausanne, Switzerland.

Erich Bornberg-Bauer (E)

Institute for Evolution and Biodiversity, University of Münsterss, 48149, Münster, Germany.
Institute for Bioinformatics and Chemoinformatics, University of Hamburg, Hamburg, Germany.
Department Protein Evolution, Max Planck Institute for Developmental Biology, Tübingen, Germany.

Matthew W Hahn (MW)

Department of Biology and Department of Computer Science, Indiana University, Bloomington, IN, USA.

Stephen Richards (S)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA. srichards@ucdavis.edu.
Present Address: UC Davis Genome Center, University of California, Davis, CA, 95616, USA. srichards@ucdavis.edu.

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