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      The genomes of two key bumblebee species with primitive eusocial organization

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      Genome Biology

      BioMed Central

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          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.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13059-015-0623-3) contains supplementary material, which is available to authorized users.

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          Most cited references 155

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          SMART, a simple modular architecture research tool: identification of signaling domains.

          Accurate multiple alignments of 86 domains that occur in signaling proteins have been constructed and used to provide a Web-based tool (SMART: simple modular architecture research tool) that allows rapid identification and annotation of signaling domain sequences. The majority of signaling proteins are multidomain in character with a considerable variety of domain combinations known. Comparison with established databases showed that 25% of our domain set could not be deduced from SwissProt and 41% could not be annotated by Pfam. SMART is able to determine the modular architectures of single sequences or genomes; application to the entire yeast genome revealed that at least 6.7% of its genes contain one or more signaling domains, approximately 350 greater than previously annotated. The process of constructing SMART predicted (i) novel domain homologues in unexpected locations such as band 4.1-homologous domains in focal adhesion kinases; (ii) previously unknown domain families, including a citron-homology domain; (iii) putative functions of domain families after identification of additional family members, for example, a ubiquitin-binding role for ubiquitin-associated domains (UBA); (iv) cellular roles for proteins, such predicted DEATH domains in netrin receptors further implicating these molecules in axonal guidance; (v) signaling domains in known disease genes such as SPRY domains in both marenostrin/pyrin and Midline 1; (vi) domains in unexpected phylogenetic contexts such as diacylglycerol kinase homologues in yeast and bacteria; and (vii) likely protein misclassifications exemplified by a predicted pleckstrin homology domain in a Candida albicans protein, previously described as an integrin.
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            TRP channels.

            The TRP (Transient Receptor Potential) superfamily of cation channels is remarkable in that it displays greater diversity in activation mechanisms and selectivities than any other group of ion channels. The domain organizations of some TRP proteins are also unusual, as they consist of linked channel and enzyme domains. A unifying theme in this group is that TRP proteins play critical roles in sensory physiology, which include contributions to vision, taste, olfaction, hearing, touch, and thermo- and osmosensation. In addition, TRP channels enable individual cells to sense changes in their local environment. Many TRP channels are activated by a variety of different stimuli and function as signal integrators. The TRP superfamily is divided into seven subfamilies: the five group 1 TRPs (TRPC, TRPV, TRPM, TRPN, and TRPA) and two group 2 subfamilies (TRPP and TRPML). TRP channels are important for human health as mutations in at least four TRP channels underlie disease.
              • Record: found
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              • Article: not found

              The genome of the model beetle and pest Tribolium castaneum.

              Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.

                Author and article information

                Genome Biol
                Genome Biology
                BioMed Central (London )
                24 April 2015
                24 April 2015
                : 16
                : 1
                [ ]School of Biological Sciences, Illinois State University, Normal, IL 61790 USA
                [ ]Experimental Ecology, Institute of Integrative Biology, Eidgenössiche Technische Hochschule (ETH) Zürich, CH-8092 Zürich, Switzerland
                [ ]Department of Biology, East Carolina University, Greenville, NC 27858 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, Dunedin, 9054 New Zealand
                [ ]Division of Animal Sciences, Division of Plant Sciences, and MU Informatics Institute, University of Missouri, Columbia, MO 65211 USA
                [ ]Department of Biology, Georgetown University, Washington, DC 20057 USA
                [ ]School of Life Sciences, Arizona State University, Tempe, AZ 85287 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, Tuscaloosa, AL 35487 USA
                [ ]Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801 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
                [ ]Department of Genetic Medicine and Development, University of Geneva Medical School, rue Michel-Servet 1, 1211 Geneva, Switzerland
                [ ]Swiss Institute of Bioinformatics, rue Michel-Servet 1, 1211 Geneva, Switzerland
                [ ]Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street, Cambridge, MA 02139 USA
                [ ]The Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, MA 02142 USA
                [ ]Westfalian Wilhelms University, Institute of Evolution and Biodiversity, Huefferstrasse 1, 48149 Muenster, Germany
                [ ]Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Spain
                [ ]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, Berkeley, CA 94720 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, Norwich, NR4 7TJ 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, Edinburgh, EH9 3FL UK
                [ ]School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ 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, Bristol, BS8 1TQ 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, London, NW1 4RY UK
                [ ]Theoretical Biology, Institute of Integrative Biology, Eidgenössiche Technische Hochschule (ETH) Zürich, CH-8092 Zürich, Switzerland
                [ ]Swiss Institute of Bioinformatics, Lausanne, Switzerland
                [ ]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, Wooster, OH 44791 USA
                [ ]Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP 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, Greensboro, NC 27403 USA
                [ ]Institute of Biosciences & Applications, National Center for Scientific Research Demokritos, Athens, Greece
                [ ]Ludwig Maximilian University, Munich, Germany
                [ ]Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX 77030 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, Urbana, IL 61801 USA
                [ ]Molecular Genetic Technology Program, School of Health Professions, MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 2, Houston, TX 77025 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, London, E1 4NS UK
                [ ]School of Life Sciences, Guangzhou University, Guangzhou, China
                [ ]Center for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, Baltimore, MD 21205 USA
                [ ]Carl R. Woese Institute for Genomic Biology, Department of Entomology, Neuroscience Program, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801 USA
                © Sadd et al.; licensee BioMed Central. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License (, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated.

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