Sawfly Genomes Reveal Evolutionary Acquisitions That Fostered the Mega-Radiation of Parasitoid and Eusocial Hymenoptera.


Journal

Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707

Informations de publication

Date de publication:
01 07 2020
Historique:
accepted: 19 05 2020
pubmed: 23 5 2020
medline: 13 7 2021
entrez: 23 5 2020
Statut: ppublish

Résumé

The tremendous diversity of Hymenoptera is commonly attributed to the evolution of parasitoidism in the last common ancestor of parasitoid sawflies (Orussidae) and wasp-waisted Hymenoptera (Apocrita). However, Apocrita and Orussidae differ dramatically in their species richness, indicating that the diversification of Apocrita was promoted by additional traits. These traits have remained elusive due to a paucity of sawfly genome sequences, in particular those of parasitoid sawflies. Here, we present comparative analyses of draft genomes of the primarily phytophagous sawfly Athalia rosae and the parasitoid sawfly Orussus abietinus. Our analyses revealed that the ancestral hymenopteran genome exhibited traits that were previously considered unique to eusocial Apocrita (e.g., low transposable element content and activity) and a wider gene repertoire than previously thought (e.g., genes for CO2 detection). Moreover, we discovered that Apocrita evolved a significantly larger array of odorant receptors than sawflies, which could be relevant to the remarkable diversification of Apocrita by enabling efficient detection and reliable identification of hosts.

Identifiants

pubmed: 32442304
pii: 5842140
doi: 10.1093/gbe/evaa106
pmc: PMC7455281
doi:

Substances chimiques

DNA Transposable Elements 0
Glycoproteins 0
Insect Proteins 0
MRJP1 protein, Apis mellifera 0
Receptors, Odorant 0
storage proteins, Insecta 0

Types de publication

Comparative Study 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

1099-1188

Subventions

Organisme : NHGRI NIH HHS
ID : U54 HG003273
Pays : United States

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Références

PLoS Genet. 2012;8(8):e1002930
pubmed: 22952454
Genome Biol Evol. 2015 Aug 12;7(8):2407-16
pubmed: 26272716
J Insect Physiol. 2012 Apr;58(4):473-87
pubmed: 22100291
Science. 2011 Mar 18;331(6023):1386
pubmed: 21415334
Dev Biol. 2015 Mar 1;399(1):154-163
pubmed: 25592223
Mol Biol Evol. 2000 Apr;17(4):540-52
pubmed: 10742046
Science. 2007 Jul 6;317(5834):86-94
pubmed: 17615350
Genome Biol. 2016 Oct 11;17(1):211
pubmed: 27802837
Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5667-72
pubmed: 21282651
Bioinformatics. 2007 Nov 1;23(21):2947-8
pubmed: 17846036
Curr Opin Insect Sci. 2018 Feb;25:65-75
pubmed: 29602364
BMC Evol Biol. 2019 Jan 9;19(1):11
pubmed: 30626321
Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):18012-7
pubmed: 23071321
Heredity (Edinb). 2010 Mar;104(3):270-7
pubmed: 20087393
Nature. 2008 Aug 21;454(7207):955-60
pubmed: 18719581
BMC Genomics. 2015 Aug 07;16:583
pubmed: 26251035
PLoS One. 2012;7(9):e45125
pubmed: 22984621
Genome Res. 2007 Dec;17(12):1898-908
pubmed: 17989259
Nat Biotechnol. 2010 May;28(5):511-5
pubmed: 20436464
Bioinformatics. 2008 Mar 1;24(5):637-44
pubmed: 18218656
Nucleic Acids Res. 2011 Jul;39(Web Server issue):W470-4
pubmed: 21646336
Insect Mol Biol. 2010 Jun 1;19(3):337-46
pubmed: 20201980
PLoS Biol. 2014 Nov 25;12(11):e1002005
pubmed: 25423365
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Nature. 2012 Oct 4;490(7418):49-54
pubmed: 22992520
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Chromosome Res. 2011 Aug;19(6):809-23
pubmed: 21877225
Curr Opin Struct Biol. 2016 Jun;38:44-52
pubmed: 27309309
Integr Comp Biol. 2015 Nov;55(5):830-42
pubmed: 26319405
Mol Ecol. 2016 Apr;25(8):1769-84
pubmed: 26859767
Annu Rev Entomol. 1998;43:129-51
pubmed: 9444751
Am Nat. 1998 Oct;152(4):635-51
pubmed: 18811369
Genome Res. 2006 Nov;16(11):1385-94
pubmed: 17065613
Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6815-9
pubmed: 9192648
Genome Res. 2006 Nov;16(11):1334-8
pubmed: 17065606
Cytogenet Genome Res. 2005;110(1-4):462-7
pubmed: 16093699
Science. 2015 Jun 5;348(6239):1139-43
pubmed: 25977371
Genome Res. 2011 Aug;21(8):1339-48
pubmed: 21719571
BMC Bioinformatics. 2005 Feb 15;6:31
pubmed: 15713233
Insect Mol Biol. 2006 Oct;15(5):645-56
pubmed: 17069638
Nucleic Acids Res. 2008 Jun;36(10):3420-35
pubmed: 18445632
J Comp Physiol A. 1992 Jan;170(1):23-40
pubmed: 1573568
Nature. 2011 Nov 23;479(7374):487-92
pubmed: 22113690
Nat Commun. 2017 Aug 17;8(1):297
pubmed: 28819196
Methods. 2016 Jan 15;93:15-23
pubmed: 26318087
Science. 2006 Nov 10;314(5801):941-52
pubmed: 17095691
J Chem Ecol. 2012 Nov;38(11):1366-75
pubmed: 23053922
Mol Biol Evol. 2016 Jun;33(6):1635-8
pubmed: 26921390
Insect Biochem Mol Biol. 2012 Sep;42(9):647-54
pubmed: 22617191
Bioinformatics. 2007 Jan 15;23(2):257-8
pubmed: 17098774
PLoS One. 2010 Jan 19;5(1):e8597
pubmed: 20087411
Naturwissenschaften. 2005 Oct;92(10):464-7
pubmed: 16136295
PeerJ. 2016 Sep 06;4:e2427
pubmed: 27651995
Nature. 2008 Apr 24;452(7190):949-55
pubmed: 18362917
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W182-5
pubmed: 17526522
Nucleic Acids Res. 2012 Jan;40(Database issue):D130-5
pubmed: 22121212
Syst Biol. 2002 Jun;51(3):492-508
pubmed: 12079646
Nucleic Acids Res. 2019 Jan 8;47(D1):D351-D360
pubmed: 30398656
Mol Biol Evol. 2012 Feb;29(2):787-96
pubmed: 22016574
BMC Genomics. 2017 Jul 17;18(1):535
pubmed: 28716078
Nature. 2008 Jun 19;453(7198):1064-71
pubmed: 18563158
Bioinformatics. 2015 Oct 1;31(19):3210-2
pubmed: 26059717
Nature. 2006 Oct 26;443(7114):931-49
pubmed: 17073008
Genome Res. 2008 Jan;18(1):188-96
pubmed: 18025269
Arthropod Struct Dev. 2011 Jan;40(1):2-20
pubmed: 20951828
Heredity (Edinb). 2007 Apr;98(4):189-97
pubmed: 17389895
Dev Genes Evol. 2004 Mar;214(3):128-33
pubmed: 14872342
Science. 2010 Jan 15;327(5963):343-8
pubmed: 20075255
Bioinformatics. 2007 May 1;23(9):1061-7
pubmed: 17332020
Genome Res. 2006 Nov;16(11):1395-403
pubmed: 17065611
Nat Commun. 2014 May 20;5:3636
pubmed: 24845553
Brief Bioinform. 2016 Sep;17(5):877-90
pubmed: 26454094
Appl Entomol Zool. 2017;52(3):497-509
pubmed: 28798494
Science. 2010 Aug 27;329(5995):1068-71
pubmed: 20798317
BMC Evol Biol. 2014 Mar 20;14(1):52
pubmed: 24646345
Insect Biochem Mol Biol. 2007 Oct;37(10):1064-74
pubmed: 17785194
Mol Biol Evol. 2013 Dec;30(12):2725-9
pubmed: 24132122
Genome Res. 2005 Mar;15(3):343-51
pubmed: 15710750
Trends Genet. 2007 Jan;23(1):16-20
pubmed: 17097187
Genome Biol. 2013 Dec 20;14(12):R142
pubmed: 24359881
Insect Biochem Mol Biol. 2005 Dec;35(12):1367-77
pubmed: 16291092
PLoS One. 2013 Dec 27;8(12):e83984
pubmed: 24386321
Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5673-8
pubmed: 21282631
Genome Biol. 2015 Apr 24;16:76
pubmed: 25908251
Nucleic Acids Res. 2015 Jan;43(Database issue):D714-9
pubmed: 25332403
Nat Genet. 2013 May;45(5):495-500
pubmed: 23525074
Nature. 2010 Aug 5;466(7307):720-6
pubmed: 20686567
Nature. 2013 Jan 24;493(7433):526-31
pubmed: 23254933
Mol Biol Evol. 2015 Jan;32(1):268-74
pubmed: 25371430
Genome Res. 2002 Apr;12(4):656-64
pubmed: 11932250
Trends Genet. 2012 Jan;28(1):14-21
pubmed: 21982512
Proc Natl Acad Sci U S A. 2011 Jan 25;108(4):1513-8
pubmed: 21187386
Science. 1998 Dec 11;282(5396):2012-8
pubmed: 9851916
Nature. 2007 Jan 4;445(7123):86-90
pubmed: 17167414
Genome Biol. 2007;8(3):R41
pubmed: 17374142
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
Science. 2002 Dec 13;298(5601):2157-67
pubmed: 12481130
Nucleic Acids Res. 2016 Jan 4;44(D1):D279-85
pubmed: 26673716
Biol Rev Camb Philos Soc. 2014 May;89(2):255-69
pubmed: 23855350
Curr Biol. 2017 Apr 3;27(7):1013-1018
pubmed: 28343967
Nucleic Acids Res. 2003 Nov 15;31(22):6633-9
pubmed: 14602924
Insect Mol Biol. 2010 Feb;19 Suppl 1:137-46
pubmed: 20167024
Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3574-8
pubmed: 17360684
Nature. 2001 Feb 15;409(6822):860-921
pubmed: 11237011
Genome Biol Evol. 2018 Nov 1;10(11):2997-3011
pubmed: 30335145
Genome Biol. 2013 Apr 25;14(4):R36
pubmed: 23618408
Bioinformatics. 2011 Mar 15;27(6):764-70
pubmed: 21217122
Nature. 2017 May 18;545(7654):340-344
pubmed: 28489826
Genome Biol. 2013 Aug 30;14(8):R93
pubmed: 24000942
Nucleic Acids Res. 2017 Jan 4;45(D1):D744-D749
pubmed: 27899580
Mol Biol Evol. 2017 Sep 1;34(9):2422-2424
pubmed: 28472384
Mol Biol Evol. 2013 Aug;30(8):1987-97
pubmed: 23709260
J Exp Biol. 2014 Mar 15;217(Pt 6):1003-8
pubmed: 24311804
Nature. 2009 Jul 16;460(7253):352-8
pubmed: 19606141
Annu Rev Entomol. 2008;53:361-85
pubmed: 17877453
Nat Methods. 2017 Jun;14(6):587-589
pubmed: 28481363
Insect Mol Biol. 2010 Feb;19 Suppl 1:121-36
pubmed: 20167023
BMC Mol Biol. 2010 Mar 26;11:23
pubmed: 20346164
Mol Biol Evol. 2009 Jun;26(6):1273-87
pubmed: 19252076
Genesis. 2003 Mar;35(3):185-91
pubmed: 12640624
Bioinformatics. 2004 Jan 22;20(2):289-90
pubmed: 14734327
Proc Natl Acad Sci U S A. 2010 May 11;107(19):8677-82
pubmed: 20421492
Genome Biol. 2015 Apr 24;16:83
pubmed: 25908406
Syst Biol. 2006 Aug;55(4):539-52
pubmed: 16785212
Toxins (Basel). 2015 Apr 01;7(4):1126-50
pubmed: 25835385
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Syst Biol. 2010 May;59(3):307-21
pubmed: 20525638
J Hered. 2013 Sep-Oct;104(5):595-600
pubmed: 23940263
BMC Bioinformatics. 2004 May 14;5:59
pubmed: 15144565
Database (Oxford). 2011 Apr 07;2011:bar008
pubmed: 21474551
Nature. 2002 Dec 5;420(6915):520-62
pubmed: 12466850

Auteurs

Jan Philip Oeyen (JP)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.
Lead Contact.

Patrice Baa-Puyoulet (P)

INSA-Lyon, INRAE, BF2I, UMR0203, Université de Lyon, Villeurbanne, France.

Joshua B Benoit (JB)

Department of Biological Sciences, University of Cincinnati.

Leo W Beukeboom (LW)

Groningen Institute for Evolutionary Life Sciences, University of Groningen, The Netherlands.

Erich Bornberg-Bauer (E)

Institute for Evolution and Biodiversity, University of Münster, Germany.

Anja Buttstedt (A)

B CUBE-Center for Molecular Bioengineering, Technische Universität Dresden, Germany.

Federica Calevro (F)

INSA-Lyon, INRAE, BF2I, UMR0203, Université de Lyon, Villeurbanne, France.

Elizabeth I Cash (EI)

School of Life Sciences, College of Liberal Arts and Sciences, Arizona State University.
Department of Environmental Science, Policy, and Management, College of Natural Resources, University of California, Berkeley.

Hsu Chao (H)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Hubert Charles (H)

INSA-Lyon, INRAE, BF2I, UMR0203, Université de Lyon, Villeurbanne, France.

Mei-Ju May Chen (MM)

Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, Taipei, Taiwan.

Christopher Childers (C)

USDA-ARS, National Agricultural Library, Beltsville, Maryland.

Andrew G Cridge (AG)

Genomics Aotearoa and Biochemistry Department, University of Otago, Dunedin, New Zealand.

Peter Dearden (P)

Genomics Aotearoa and Biochemistry Department, University of Otago, Dunedin, New Zealand.

Huyen Dinh (H)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Harsha Vardhan Doddapaneni (HV)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Amanda Dolan (A)

Department of Biology, University of Rochester.

Alexander Donath (A)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.

Daniel Dowling (D)

Institute for Evolution and Biodiversity, University of Münster, Germany.

Shannon Dugan (S)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Elizabeth Duncan (E)

School of Biology, Faculty of Biological Sciences, University of Leeds, United Kingdom.

Elena N Elpidina (EN)

A.N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Russia.

Markus Friedrich (M)

Department of Biological Sciences, Wayne State University, Detroit.

Elzemiek Geuverink (E)

Groningen Institute for Evolutionary Life Sciences, University of Groningen, The Netherlands.

Joshua D Gibson (JD)

Department of Biology, Georgia Southern University, Statesboro.
Department of Entomology, Purdue University, West Lafayette.

Sonja Grath (S)

Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany.

Cornelis J P Grimmelikhuijzen (CJP)

Department of Biology, University of Copenhagen, Denmark.

Ewald Große-Wilde (E)

Department of Evolutionary Neuroethology, Max-Planck-Institute for Chemical Ecology, Jena, Germany.
Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague (CULS), Praha 6-Suchdol, Czech Republic.

Cameron Gudobba (C)

Department of Psychiatry and Behavioral Neuroscience, University of Chicago.

Yi Han (Y)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Bill S Hansson (BS)

Department of Evolutionary Neuroethology, Max-Planck-Institute for Chemical Ecology, Jena, Germany.

Frank Hauser (F)

Department of Biology, University of Copenhagen, Denmark.

Daniel S T Hughes (DST)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Panagiotis Ioannidis (P)

Department of Genetic Medicine and Development, University of Geneva Medical School, Switzerland.
Swiss Institute of Bioinformatics, Geneva, Switzerland.
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Crete, Greece.

Emmanuelle Jacquin-Joly (E)

INRAE, CNRS, IRD, UPEC, Univ. P7, Institute of Ecology and Environmental Sciences of Paris, Sorbonne Université, Versailles, France.

Emily C Jennings (EC)

Department of Biological Sciences, University of Cincinnati.

Jeffery W Jones (JW)

Department of Biological Sciences, Oakland University, Rochester.

Steffen Klasberg (S)

Institute for Evolution and Biodiversity, University of Münster, Germany.

Sandra L Lee (SL)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Peter Lesný (P)

Institute of Evolutionary Biology and Ecology, Zoology and Evolutionary Biology, University of Bonn, Germany.

Mackenzie Lovegrove (M)

Genomics Aotearoa and Biochemistry Department, University of Otago, Dunedin, New Zealand.

Sebastian Martin (S)

Institute of Evolutionary Biology and Ecology, Zoology and Evolutionary Biology, University of Bonn, Germany.

Alexander G Martynov (AG)

Center of Life Sciences, Skolkovo Institute of Science and Technology, Russia.

Christoph Mayer (C)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.

Nicolas Montagné (N)

INRAE, CNRS, IRD, UPEC, Univ. P7, Institute of Ecology and Environmental Sciences of Paris, Sorbonne Université, Paris, France.

Victoria C Moris (VC)

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

Monica Munoz-Torres (M)

Berkeley Bioinformatics Open-source Projects (BBOP), Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California.

Shwetha Canchi Murali (SC)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Donna M Muzny (DM)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Brenda Oppert (B)

USDA Agricultural Research Service, Center for Grain and Animal Health Research, Manhattan, Kansas.

Nicolas Parisot (N)

INSA-Lyon, INRAE, BF2I, UMR0203, Université de Lyon, Villeurbanne, France.

Thomas Pauli (T)

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

Ralph S Peters (RS)

Arthropoda Department, Center for Taxonomy and Evolutionary Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.

Malte Petersen (M)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.
Max Planck Institute of Immunobiology and Epigenetics, Freiburg, Germany.

Christian Pick (C)

Zoological Institute, University of Hamburg, Germany.

Emma Persyn (E)

INRAE, CNRS, IRD, UPEC, Univ. P7, Institute of Ecology and Environmental Sciences of Paris, Sorbonne Université, Paris, France.

Lars Podsiadlowski (L)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.

Monica F Poelchau (MF)

USDA-ARS, National Agricultural Library, Beltsville, Maryland.

Panagiotis Provataris (P)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.

Jiaxin Qu (J)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Maarten J M F Reijnders (MJMF)

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

Björn Marcus von Reumont (BM)

Institute for Insect Biotechnology, University of Gießen, Germany.
Center for Translational Biodiversity Genomics (LOEWE-TBG), Frankfurt, Germany.

Andrew J Rosendale (AJ)

Department of Biological Sciences, University of Cincinnati.

Felipe A Simao (FA)

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

John Skelly (J)

Genomics Aotearoa and Biochemistry Department, University of Otago, Dunedin, New Zealand.

Alexandros G Sotiropoulos (AG)

Department of Biology, University of Copenhagen, Denmark.

Aaron L Stahl (AL)

Department of Biological Sciences, University of Cincinnati.
Department of Neuroscience, The Scripps Research Institute, Jupiter, Florida.

Megumi Sumitani (M)

Transgenic Silkworm Research Unit, Division of Biotechnology, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Owashi, Tsukuba, Japan.

Elise M Szuter (EM)

School of Life Sciences, College of Liberal Arts and Sciences, Arizona State University.

Olivia Tidswell (O)

Biochemistry Department, University of Otago, Dunedin, New Zealand.
Zoology Department, University of Cambridge, United Kingdom.

Evangelos Tsitlakidis (E)

Department of Biology, University of Copenhagen, Denmark.

Lucia Vedder (L)

Center for Bioinformatics Tübingen (ZBIT), University of Tübingen, Germany.

Robert M Waterhouse (RM)

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

John H Werren (JH)

Department of Biology, University of Rochester.

Jeanne Wilbrandt (J)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.
Computational Biology Group, Leibniz Institute on Aging-Fritz Lipmann Institute, Jena, Germany.

Kim C Worley (KC)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Daisuke S Yamamoto (DS)

Division of Medical Zoology, Department of Infection and Immunity, Jichi Medical University, Yakushiji, Shimotsuke, Japan.

Louis van de Zande (L)

Groningen Institute for Evolutionary Life Sciences, University of Groningen, The Netherlands.

Evgeny M Zdobnov (EM)

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

Tanja Ziesmann (T)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.

Richard A Gibbs (RA)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Stephen Richards (S)

Human Genome Sequencing Center, Department of Human and Molecular Genetics, Baylor College of Medicine, Houston, Texas.

Masatsugu Hatakeyama (M)

Insect Genome Research and Engineering Unit, Division of Applied Genetics, Institute of Agrobiological Sciences, NARO, Owashi, Tsukuba, Japan.

Bernhard Misof (B)

Center for Molecular Biodiversity Research, Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany.

Oliver Niehuis (O)

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

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH