The genomes of two key bumblebee species with primitive eusocial organization View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2015-04-24

AUTHORS

Ben M Sadd, Seth M Barribeau, Guy Bloch, Dirk C de Graaf, Peter Dearden, Christine G Elsik, Jürgen Gadau, Cornelis JP 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 MG Bitondi, Mark L Blaxter, Andrew FG Bourke, Mark JF 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 CP 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 FA Moritz, Ajay Nair, Kathrin Näpflin, Inga Nissen, Jinzhi Niu, Francis MF 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 LP Simões, Michelle PM 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 KO 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

ABSTRACT

BackgroundThe 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.ResultsWe 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.ConclusionsThese 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. More... »

PAGES

76

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  • Journal

    TITLE

    Genome Biology

    ISSUE

    1

    VOLUME

    16

    Author Affiliations

  • Experimental Ecology, Institute of Integrative Biology, Eidgenössiche Technische Hochschule (ETH) Zürich, CH-8092, Zürich, Switzerland
  • Department of Biology, East Carolina University, 27858, Greenville, NC, USA
  • Department of Ecology, Evolution, and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
  • Laboratory of Zoophysiology, Faculty of Sciences, Ghent University, Krijgslaan 281, S2, 9000, Ghent, Belgium
  • Laboratory for Evolution and Development, Genetics Otago and the National Research Centre for Growth and Development, Department of Biochemistry, University of Otago, P.O. Box 56, 9054, Dunedin, New Zealand
  • Department of Biology, Georgetown University, 20057, Washington, DC, USA
  • School of Life Sciences, Arizona State University, 85287, Tempe, AZ, USA
  • Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, Copenhagen, Denmark
  • University of Hohenheim, Institute of Animal Science, Garbenstrasse 17, 70599, Stuttgart, Germany
  • Department of Biological Sciences, University of Alabama, 35487, Tuscaloosa, AL, USA
  • Department of Entomology, University of Illinois at Urbana-Champaign, 61801, Urbana, IL, USA
  • Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium
  • Institute of Biology, Martin-Luther-University Halle-Wittenberg, Wittenberg, Germany
  • The Broad Institute of MIT and Harvard, 7 Cambridge Center, 02142, Cambridge, MA, USA
  • Westfalian Wilhelms University, Institute of Evolution and Biodiversity, Huefferstrasse 1, 48149, Muenster, Germany
  • Universitat Pompeu Fabra (UPF), Barcelona, Spain
  • Ernst Moritz Arndt University Greifswald, Institute for Mathematics and Computer Science, Walther-Rathenau-Str. 47, 17487, Greifswald, Germany
  • Genomics Division, Lawrence Berkeley National Laboratory, 94720, Berkeley, CA, USA
  • National Center for Biotechnology Information, National Library of Medicine, Bethesda, USA
  • Department of Chemistry, Biotechnology and Food Science, Norwegian University of Food Science, N-1432, Aas, Norway
  • School of Computing Sciences, University of East Anglia, Norwich Research Park, NR4 7TJ, Norwich, UK
  • Institute of Evolutionary Genetics, Heinrich Heine University Duesseldorf, Universitaetsstrasse 1, 40225, Duesseldorf, Germany
  • University of Cologne, Institute of Genetics, Cologne, Germany
  • Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901, Ribeirão Preto, Brazil
  • Institute of Evolutionary Biology and Edinburgh Genomics, The Ashworth Laboratories, The King’s Buildings, University of Edinburgh, EH9 3FL, Edinburgh, UK
  • School of Biological Sciences, University of East Anglia, Norwich Research Park, NR4 7TJ, Norwich, UK
  • School of Biological Sciences, Royal Holloway University of London, London, UK
  • Maynooth University Department of Biology, Maynooth University, Co, Kildare, Ireland
  • School of Biological Sciences, University of Bristol, 24 Tyndall Avenue, BS8 1TQ, Bristol, UK
  • Land and Water Flagship CSIRO, Canberra, Australia
  • Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin, Ireland
  • Institute of Zoology, Zoological Society of London, Regent’s Park, NW1 4RY, London, UK
  • Computational Evolution, Department of Biosystems Science and Engineering, ETH Zürich, Basel, Switzerland
  • USDA-ARS Bee Research Laboratory, Maryland, USA
  • Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, 14040-900, Ribeirão Preto, Brazil
  • Center for Research in Scientific Computation, North Carolina State University Raleigh, Raleigh, NC, USA
  • Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Kyoto, Japan
  • Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, 14040-900, Ribeirão Preto, Brazil
  • Instituto Federal de Educação, Ciência e Tecnologia de São Paulo, 15991-502, Matão, Brazil
  • Department of Entomology, The Ohio State University, 44791, Wooster, OH, USA
  • Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, OX3 0BP, Oxford, UK
  • Department of Biological Sciences, Xi’an Jiaotong-Liverpool University, Suzhou, China
  • Department of Laboratory Medicine, University Hospital Halle (Saale), Halle, Germany
  • German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
  • University of Southampton, Southampton, UK
  • Department of Biology, University of Leicester, Leicester, UK
  • Departamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, 13565-905, São Carlos, Brazil
  • Departamento de Tecnologia, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, 14884-900, Jaboticabal, Brazil
  • Department of Biology, University of North Carolina at Greensboro, 321 McIver Street, 27403, Greensboro, NC, USA
  • Institute of Biosciences & Applications, National Center for Scientific Research Demokritos, Athens, Greece
  • Ludwig Maximilian University, Munich, Germany
  • Swiss Institute of Bioinformatics, rue Michel-Servet 1, 1211, Geneva, Switzerland
  • Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, 77030, Houston, TX, USA
  • Roy J. Carver Biotechnology Center, University of Illinois Urbana-Champaign, Urbana, IL, USA
  • Department of Crop Sciences and Institute of Genomic Biology, University of Illinois at Urbana-Champaign, 61801, Urbana, IL, USA
  • Molecular Genetic Technology Program, School of Health Professions, MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 2, 77025, Houston, TX, USA
  • Department of Human Genetics, University of Chicago, Chicago, IL, USA
  • Laboratory of Protein Biochemistry and Biomolecular Engineering, Department of Biochemistry and Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium
  • Department of Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, E1 4NS, London, UK
  • School of Life Sciences, Guangzhou University, Guangzhou, China
  • Center for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, 21205, Baltimore, MD, USA
  • Carl R. Woese Institute for Genomic Biology, Department of Entomology, Neuroscience Program, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, 61801, Urbana, IL, USA
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1186/s13059-015-0623-3

    DOI

    http://dx.doi.org/10.1186/s13059-015-0623-3

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1051567373

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/25908251


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    88 schema:description BackgroundThe 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.ResultsWe 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.ConclusionsThese 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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