The genomes of two key bumblebee species with primitive eusocial organization

Ben M Sadd; Seth M Barribeau; Guy Bloch; Dirk C de Graaf; Peter Dearden; Christine G Elsik; Jürgen Gadau; Cornelis J P Grimmelikhuijzen; Martin Hasselmann; Jeffrey D Lozier; Hugh M Robertson; Guy Smagghe; Eckart Stolle; Matthias Van Vaerenbergh; Robert M Waterhouse; Erich Bornberg-Bauer; Steffen Klasberg; Anna K Bennett; Francisco Câmara; Roderic Guigó; Katharina Hoff; Marco Mariotti; Monica Munoz-Torres; Terence Murphy; Didac Santesmasses; Gro V Amdam; Matthew Beckers; Martin Beye; Matthias Biewer; Márcia M G Bitondi; Mark L Blaxter; Andrew F G Bourke; Mark J F Brown; Severine D Buechel; Rossanah Cameron; Kaat Cappelle; James C Carolan; Olivier Christiaens; Kate L Ciborowski; David F Clarke; Thomas J Colgan; David H Collins; Andrew G Cridge; Tamas Dalmay; Stephanie Dreier; Louis du Plessis; Elizabeth Duncan; Silvio Erler; Jay Evans; Tiago Falcon; Kevin Flores; Flávia C P Freitas; Taro Fuchikawa; Tanja Gempe; Klaus Hartfelder; Frank Hauser; Sophie Helbing; Fernanda C Humann; Frano Irvine; Lars S Jermiin; Claire E Johnson; Reed M Johnson; Andrew K Jones; Tatsuhiko Kadowaki; Jonathan H Kidner; Vasco Koch; Arian Köhler; F Bernhard Kraus; H Michael G Lattorff; Megan Leask; Gabrielle A Lockett; Eamonn B Mallon; David S Marco Antonio; Monika Marxer; Ivan Meeus; Robin F A Moritz; Ajay Nair; Kathrin Näpflin; Inga Nissen; Jinzhi Niu; Francis M F Nunes; John G Oakeshott; Amy Osborne; Marianne Otte; Daniel G Pinheiro; Nina Rossié; Olav Rueppell; Carolina G Santos; Regula Schmid-Hempel; Björn D Schmitt; Christina Schulte; Zilá L P Simões; Michelle P M Soares; Luc Swevers; Eva C Winnebeck; Florian Wolschin; Na Yu; Evgeny M Zdobnov; Peshtewani K Aqrawi; Kerstin P Blankenburg; Marcus Coyle; Liezl Francisco; Alvaro G Hernandez; Michael Holder; Matthew E Hudson; LaRonda Jackson; Joy Jayaseelan; Vandita Joshi; Christie Kovar; Sandra L Lee; Robert Mata; Tittu Mathew; Irene F Newsham; Robin Ngo; Geoffrey Okwuonu; Christopher Pham; Ling-Ling Pu; Nehad Saada; Jireh Santibanez; DeNard Simmons; Rebecca Thornton; Aarti Venkat; Kimberly K O Walden; Yuan-Qing Wu; Griet Debyser; Bart Devreese; Claire Asher; Julie Blommaert; Ariel D Chipman; Lars Chittka; Bertrand Fouks; Jisheng Liu; Meaghan P O'Neill; Seirian Sumner; Daniela Puiu; Jiaxin Qu; Steven L Salzberg; Steven E Scherer; Donna M Muzny; Stephen Richards; Gene E Robinson; Richard A Gibbs; Paul Schmid-Hempel; Kim C Worley

doi:10.1186/s13059-015-0623-3

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The genomes of two key bumblebee species with primitive eusocial organization

Journal article

Open access

Peer reviewed

The genomes of two key bumblebee species with primitive eusocial organization

Ben M Sadd, Seth M Barribeau, Guy Bloch, Dirk C de Graaf, Peter Dearden, Christine G Elsik, Jürgen Gadau, Cornelis J P Grimmelikhuijzen, Martin Hasselmann, Jeffrey D Lozier, …

Genome biology, Vol.16(1), pp.76-76

24/04/2015

DOI: https://doi.org/10.1186/s13059-015-0623-3

PMCID: PMC4414376

PMID: 25908251

Abstract

Animals

Bee Venoms - genetics

Bees - classification

Bees - genetics

Bees - physiology

Behavior, Animal

Chemoreceptor Cells - metabolism

Chromosome Mapping

Databases, Genetic

Evolution, Molecular

Female

Gene Expression Regulation

Gene Rearrangement

Genes, Insect

Genomics

Interspersed Repetitive Sequences

Male

Open Reading Frames

Polymorphism, Single Nucleotide

Selenoproteins - genetics

Selenoproteins - metabolism

Sequence Analysis, DNA

Social Behavior

Species Specificity

Synteny

The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.

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Title: The genomes of two key bumblebee species with primitive eusocial organization
Creators: Ben M Sadd - Illinois State University
Seth M Barribeau - ETH Zurich
Guy Bloch - Hebrew University of Jerusalem
Dirk C de Graaf - Ghent University
Peter Dearden - University of Otago
Christine G Elsik - University of Missouri
Jürgen Gadau - Arizona State University
Cornelis J P Grimmelikhuijzen - University of Copenhagen
Martin Hasselmann - University of Hohenheim
Jeffrey D Lozier - University of Alabama
Hugh M Robertson - University of Illinois Urbana-Champaign
Guy Smagghe - Ghent University
Eckart Stolle - Martin Luther University Halle-Wittenberg
Matthias Van Vaerenbergh - Ghent University
Robert M Waterhouse - SIB Swiss Institute of Bioinformatics
Erich Bornberg-Bauer - Westfalian Wilhelms University, Institute of Evolution and Biodiversity, Muenster, Germany
Steffen Klasberg - Westfalian Wilhelms University, Institute of Evolution and Biodiversity, Muenster, Germany
Anna K Bennett - Georgetown University
Francisco Câmara - Centre for Genomic Regulation
Roderic Guigó - Centre for Genomic Regulation
Katharina Hoff - University of Greifswald
Marco Mariotti - Centre for Genomic Regulation
Monica Munoz-Torres - Georgetown University
Terence Murphy - National Center for Biotechnology Information
Didac Santesmasses - Centre for Genomic Regulation
Gro V Amdam - Arizona State University
Matthew Beckers - University of East Anglia
Martin Beye - Heinrich Heine University Düsseldorf
Matthias Biewer - University of Hohenheim
Márcia M G Bitondi - Universidade de Ribeirão Preto
Mark L Blaxter - Edinburgh Genomics
Andrew F G Bourke - University of East Anglia
Mark J F Brown - Royal Holloway University of London
Severine D Buechel - ETH Zurich
Rossanah Cameron - University of Otago
Kaat Cappelle - University of Illinois Urbana-Champaign
James C Carolan - National University of Ireland, Maynooth
Olivier Christiaens - Ghent University
Kate L Ciborowski - University of Bristol
David F Clarke - CSIRO Land and Water
Thomas J Colgan - Trinity College Dublin
David H Collins - University of East Anglia
Andrew G Cridge - University of Otago
Tamas Dalmay - University of East Anglia
Stephanie Dreier - Zoological Society of London
Louis du Plessis - ETH Zurich
Elizabeth Duncan - University of Otago
Silvio Erler - Martin Luther University Halle-Wittenberg
Jay Evans - USDA-ARS Bee Research Laboratory, Maryland, USA
Tiago Falcon - Universidade de Ribeirão Preto
Kevin Flores - North Carolina State University
Flávia C P Freitas - Universidade de São Paulo
Taro Fuchikawa - Hebrew University of Jerusalem
Tanja Gempe - Heinrich Heine University Düsseldorf
Klaus Hartfelder - Universidade de São Paulo
Frank Hauser - University of Copenhagen
Sophie Helbing - Martin Luther University Halle-Wittenberg
Fernanda C Humann - Federal Institute of São Paulo
Frano Irvine - University of Otago
Lars S Jermiin - CSIRO Land and Water
Claire E Johnson - University of Illinois Urbana-Champaign
Reed M Johnson - The Ohio State University
Andrew K Jones - Oxford Brookes University
Tatsuhiko Kadowaki - Xi’an Jiaotong-Liverpool University
Jonathan H Kidner - Martin Luther University Halle-Wittenberg
Vasco Koch - Heinrich Heine University Düsseldorf
Arian Köhler - Heinrich Heine University Düsseldorf
F Bernhard Kraus - Martin Luther University Halle-Wittenberg
H Michael G Lattorff - Martin Luther University Halle-Wittenberg
Megan Leask - University of Otago
Gabrielle A Lockett - University of Southampton
Eamonn B Mallon - University of Leicester
David S Marco Antonio - Universidade de Ribeirão Preto
Monika Marxer - ETH Zurich
Ivan Meeus - Ghent University
Robin F A Moritz - Martin Luther University Halle-Wittenberg
Ajay Nair - University of Otago
Kathrin Näpflin - ETH Zurich
Inga Nissen - Heinrich Heine University Düsseldorf
Jinzhi Niu - Ghent University
Francis M F Nunes - Universidade Federal de São Carlos
John G Oakeshott - CSIRO Land and Water
Amy Osborne - University of Otago
Marianne Otte - Martin Luther University Halle-Wittenberg
Daniel G Pinheiro - Universidade Estadual Paulista (Unesp)
Nina Rossié - Heinrich Heine University Düsseldorf
Olav Rueppell - University of North Carolina at Greensboro
Carolina G Santos - Universidade de São Paulo
Regula Schmid-Hempel - ETH Zurich
Björn D Schmitt - Heinrich Heine University Düsseldorf
Christina Schulte - Heinrich Heine University Düsseldorf
Zilá L P Simões - Universidade de Ribeirão Preto
Michelle P M Soares - Universidade de Ribeirão Preto
Luc Swevers - National Centre of Scientific Research "Demokritos"
Eva C Winnebeck - Ludwig-Maximilians-Universität München
Florian Wolschin - Arizona State University
Na Yu - Ghent University
Evgeny M Zdobnov - University of Geneva
Peshtewani K Aqrawi - Baylor Genetics
Kerstin P Blankenburg - Baylor Genetics
Marcus Coyle - Baylor College of Medicine
Liezl Francisco - Baylor College of Medicine
Alvaro G Hernandez - University of Illinois Urbana-Champaign
Michael Holder - Baylor College of Medicine
Matthew E Hudson - University of Illinois at Urbana Champaign
LaRonda Jackson - Baylor College of Medicine
Joy Jayaseelan - Baylor College of Medicine
Vandita Joshi - Baylor College of Medicine
Christie Kovar - Baylor College of Medicine
Sandra L Lee - Baylor College of Medicine
Robert Mata - Baylor College of Medicine
Tittu Mathew - Baylor College of Medicine
Irene F Newsham - Molecular Genetic Technology Program, School of Health Professions, MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 2, Houston, TX, 77025, USA. inewsham@mdanderson.org
Robin Ngo - Baylor College of Medicine
Geoffrey Okwuonu - Baylor College of Medicine
Christopher Pham - Baylor College of Medicine
Ling-Ling Pu - Baylor College of Medicine
Nehad Saada - Baylor College of Medicine
Jireh Santibanez - Baylor College of Medicine
DeNard Simmons - Baylor College of Medicine
Rebecca Thornton - Baylor College of Medicine
Aarti Venkat - University of Chicago
Kimberly K O Walden - University of Illinois at Urbana Champaign
Yuan-Qing Wu - Baylor College of Medicine
Griet Debyser - Ghent University
Bart Devreese - Ghent University
Claire Asher - Zoological Society of London
Julie Blommaert - University of Otago
Ariel D Chipman - Hebrew University of Jerusalem
Lars Chittka - Queen Mary University of London
Bertrand Fouks - University of North Carolina at Greensboro
Jisheng Liu - Guangzhou University
Meaghan P O'Neill - University of Otago
Seirian Sumner - University of Bristol
Daniela Puiu - Johns Hopkins University
Jiaxin Qu - Baylor College of Medicine
Steven L Salzberg - Johns Hopkins University
Steven E Scherer - Guangzhou University
Donna M Muzny - Baylor College of Medicine
Stephen Richards - Baylor College of Medicine
Gene E Robinson - University of Illinois at Urbana Champaign
Richard A Gibbs - Baylor College of Medicine
Paul Schmid-Hempel - Experimental Ecology, Institute of Integrative Biology, Eidgenössiche Technische Hochschule (ETH) Zürich, CH-8092, Zürich, Switzerland. psh@env.ethz.ch
Kim C Worley - Baylor College of Medicine
Publication Details: Genome biology, Vol.16(1), pp.76-76
Date published: 24/04/2015
Grant note: U54 HG003273 / NHGRI NIH HHS R01 HG006677 / NHGRI NIH HHS MR/K001744/1 / Medical Research Council BB/G00661X/1 / Biotechnology and Biological Sciences Research Council 095831 / Wellcome Trust DP1 OD006416 / NIH HHS G0900740 / Medical Research Council
Identifiers: 99783383002346
Academic Unit: School of Biosciences
Language: English
Resource Type: Journal article

The genomes of two key bumblebee species with primitive eusocial organization

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