Article
Nature 443, 931-949 (26 October 2006) | doi:10.1038/nature05260; Received 13 July 2006; Accepted 19 September 2006
There is a Corrigendum (23 November 2006) associated with this document.
Insights into social insects from the genome of the honeybee Apis mellifera
Overall project leadership:, George M. Weinstock1,2, Gene E. Robinson7,9,13,14, Principal investigators:, Richard A. Gibbs1,2, George M. Weinstock1,2, Community coordination:, George M. Weinstock, leader1,2, Gene E. Robinson, leader7,9,13,14, Kim C. Worley, leader1,2, Jay D. Evans4, Ryszard Maleszka6, Hugh M. Robertson7,9,13,14, Daniel B. Weaver16, Annotation section leaders:, Martin Beye17, Peer Bork18,19, Christine G. Elsik20, Jay D. Evans4, Klaus Hartfelder25, Greg J. Hunt27, Hugh M. Robertson7,9,13,14, Gene E. Robinson7,9,13,14, Ryszard Maleszka6, George M. Weinstock1,2, Kim C. Worley1,2, Evgeny M. Zdobnov18,28, Caste development and reproduction:, Klaus Hartfelder, leader25, Gro V. Amdam29, Mrcia M. G. Bitondi26, Anita M. Collins4, Alexandre S. Cristino30, Jay D. Evans4, H. Michael31, G. Lattorff31, Carlos H. Lobo24, Robin F. A. Moritz31, Francis M. F. Nunes24, Robert E. Page, Jr29, Zil L. P. Sim|[otilde]|es26, Diana Wheeler32, EST sequencing:, Piero Carninci, leader33, Shiro Fukuda33, Yoshihide Hayashizaki33, Chikatoshi Kai33, Jun Kawai33, Naoko Sakazume33, Daisuke Sasaki33, Michihira Tagami33, Brain and behaviour:, Ryszard Maleszka, leader6, Gro V. Amdam29, Stefan Albert34, Geert Baggerman35, Kyle T. Beggs37, Guy Bloch38, Giuseppe Cazzamali41, Mira Cohen38, Mark David Drapeau42, Dorothea Eisenhardt43, Christine Emore27, Michael A. Ewing15, Susan E. Fahrbach48, Sylvain For|[ecirc]|t6, Cornelis J. P. Grimmelikhuijzen41, Frank Hauser41, Amanda B. Hummon15, Greg J. Hunt27, Jurgen Huybrechts35, Andrew K. Jones44, Tatsuhiko Kadowaki55, Noam Kaplan40, Robert Kucharski6, G|[eacute]|rard Leboulle43, Michal Linial39,40, J. Troy Littleton45, Alison R. Mercer37, Robert E. Page, Jr29, Hugh M. Robertson7,9,13,14, Gene E. Robinson7,9,13,14, Timothy A. Richmond15, Sandra L. RodriguezZas12, Elad B. Rubin38, David B. Sattelle44, David Schlipalius27, Liliane Schoofs35, Yair Shemesh38, Jonathan V. Sweedler13,15, Rodrigo Velarde7, Peter Verleyen35, Evy Vierstraete35, Michael R. Williamson41, Development and metabolism:, Martin Beye, leader17, Seth A. Ament13, Susan J. Brown50, Miguel Corona7, Peter K. Dearden36, W. Augustine Dunn52, Michelle M. Elekonich53, Christine G. Elsik20, Sylvain For|[ecirc]|t6, Tomoko Fujiyuki54, Irene Gattermeier17, Tanja Gempe17, Martin Hasselmann17, Tatsuhiko Kadowaki55, Eriko Kage54, Azusa Kamikouchi54, Takeo Kubo54, Robert Kucharski6, Takekazu Kunieda54, Marc|[eacute]| Lorenzen49, Ryszard Maleszka6, Natalia V. Milshina20, Mizue Morioka54, Kazuaki Ohashi54, Ross Overbeek57, Robert E. Page, Jr29, Hugh M. Robertson7,9,13,14, Gene E. Robinson7,9,13,14, Christian A. Ross53, Morten Schioett17, Teresa Shippy51, Hideaki Takeuchi54, Amy L. Toth14, Judith H. Willis52, Megan J. Wilson36, Comparative and evolutionary analysis:, Hugh M. Robertson, leader7,9,13,14, Evgeny M. Zdobnov, leader18,28, Peer Bork18,19, Christine G. Elsik20, Karl H. J. Gordon46, Ivica Letunic18, Funding agency management:, Kevin Hackett5, Jane Peterson58, Adam Felsenfeld58, Mark Guyer58, Physical and genetic mapping:, Michel Solignac, leader56, Richa Agarwala59, Jean Marie Cornuet60, Christine G. Elsik20, Christine Emore27, Greg J. Hunt27, Monique Monnerot56, Florence Mougel56, Justin T. Reese20, David Schlipalius27, Dominique Vautrin56, Daniel B. Weaver16, Ribosomal RNA genes and related retrotransposable elements:, Joseph J. Gillespie, leader21,62, Jamie J. Cannone61, Robin R. Gutell61, J. Spencer Johnston21, Gene prediction and consensus gene set:, Christine G. Elsik, leader20, Giuseppe Cazzamali41, Michael B. Eisen63,64, Cornelis J. P. Grimmelikhuijzen41, Frank Hauser41, Amanda B. Hummon15, Venky N. Iyer63, Vivek Iyer65, Peter Kosarev66, Aaron J. Mackey67, Ryszard Maleszka6, Justin T. Reese20, Timothy A. Richmond15, Hugh M. Robertson7,9,13,14, Victor Solovyev68, Alexandre Souvorov59, Jonathan V. Sweedler13,15, George M. Weinstock1,2, Michael R. Williamson41, Evgeny M. Zdobnov18,28, Honeybee disease and immunity:, Jay D. Evans, leader4, Katherine A. Aronstein69, Katarina Bilikova70, Yan Ping Chen4, Andrew G. Clark72, Laura I. Decanini4, William M. Gelbart73, Charles Hetru74, Dan Hultmark75, Jean-Luc Imler74, Haobo Jiang76, Michael Kanost51, Kiyoshi Kimura77, Brian P. Lazzaro71, Dawn L. Lopez4, Jozef Simuth70, Graham J. Thompson78, Zhen Zou76, BAC/fosmid library construction and analysis:, Pieter De Jong, leader79, Erica Sodergren, leader1,2, Mikl|[oacute]|s Cs|[udblac]|r|[ouml]|s87, Aleksandar Milosavljevic1,2, J. Spencer Johnston21, Kazutoyo Osoegawa79, Stephen Richards1,2, Chung-Li Shu79, George M. Weinstock1,2, G|[plus]|C content:, Christine G. Elsik, leader20, Laurent Duret80, Eran Elhaik23, Dan Graur23, Justin T. Reese20, Hugh M. Robertson7,9,13,14, Transposable elements:, Hugh M. Robertson, leader7,9,13,14, Christine G. Elsik20, Gene regulation including miRNA and RNAi:, Ryszard Maleszka, leader6, Daniel B. Weaver, leader16, Gro V. Amdam29, Juan M. Anzola20, Kathryn S. Campbell73, Kevin L. Childs20, Derek Collinge46, Madeline A. Crosby75, C. Michael Dickens20, Christine G. Elsik20, Karl H. J. Gordon46, L. Sian Gramates73, Christina M. Grozinger81, Peter L. Jones9, Mireia Jorda89, Xu Ling8, Beverly B. Matthews73, Jonathan Miller1,3, Natalia V. Milshina20, Craig Mizzen17, Miguel A. Peinado89, Justin T. Reese20, Jeffrey G. Reid3,22, Hugh M. Robertson7,9,13,14, Gene E. Robinson7,9,13,14, Susan M. Russo73, Andrew J. Schroeder73, Susan E. St Pierre73, Ying Wang9, Pinglei Zhou73, Superscaffold assembly:, Hugh M. Robertson, leader7,9,13,14, Richa Agarwala59, Christine G. Elsik20, Natalia V. Milshina20, Justin T. Reese20, Daniel B. Weaver16, Data management:, Kim C. Worley, leader1,2, Kevin L. Childs20, C. Michael Dickens20, Christine G. Elsik20, William M. Gelbart73, Huaiyang Jiang1,2, Paul Kitts59, Natalia V. Milshina20, Justin T. Reese20, Barbara Ruef59, Susan M. Russo73, Anand Venkatraman20, George M. Weinstock1,2, Lan Zhang1,2, Pinglei Zhou69, Chromosome structure:, J. Spencer Johnston, leader21, Gildardo Aquino-Perez21, Jean Marie Cornuet60, Monique Monnerot56, Michel Solignac56, Dominique Vautrin56, Population genetics and SNPs:, Charles W. Whitfield, leader7,13,14, Susanta K. Behura7, Stewart H. Berlocher7,14, Andrew G. Clark72, Richard A. Gibbs1,2, J. Spencer Johnston21, Walter S. Sheppard82, Deborah R. Smith83, Andrew V. Suarez7,11, Neil D. Tsutsui84, Daniel B. Weaver16, Xuehong Wei1,2, David Wheeler1,2, Genome assembly:, George M. Weinstock, leader1,2, Kim C. Worley, leader1,2, Paul Havlak1,2, Bingshan Li1,2, Yue Liu1,2, Erica Sodergren1,2, Lan Zhang1,2, (A|[plus]|T)-rich DNA generation:, Martin Beye, leader17, Martin Hasselmann17, Angela Jolivet1,2, Sandra Lee1,2, Lynne V. Nazareth1,2, Ling-Ling Pu1,2, Rachel Thorn1,2, George M. Weinstock1,2, Tiling arrays:, Viktor Stolc, leader85, Gene E. Robinson, leader7,9,13,14, Ryszard Maleszka6, Thomas Newman7, Manoj Samanta85,86, Waraporn A. Tongprasit85, Anti-xenobiotic defence mechanisms:, Katherine A. Aronstein, leader69, Charles Claudianos, leader6,46, May R. Berenbaum7, Sunita Biswas6,46, Dirk C. de Graaf47, Rene Feyereisen90, Reed M. Johnson7, John G. Oakeshott46, Hilary Ranson88, Mary A. Schuler10, DNA sequencing:, Donna Muzny, leader1,2, Richard A. Gibbs, leader1,2, George M. Weinstock, leader1,2, Joseph Chacko1,2, Clay Davis1,2, Huyen Dinh1,2, Rachel Gill1,2, Judith Hernandez1,2, Sandra Hines1,2, Jennifer Hume1,2, LaRonda Jackson1,2, Christie Kovar1,2, Lora Lewis1,2, George Miner1,2, Margaret Morgan1,2, Lynne V. Nazareth1,2, Ngoc Nguyen1,2, Geoffrey Okwuonu1,2, Heidi Paul1,2, Stephen Richards1,2, Jireh Santibanez1,2, Glenford Savery1,2, Erica Sodergren1,2, Amanda Svatek1,2, Donna Villasana1,2 & Rita Wright1,2 for The Honeybee Genome Sequencing Consortium
- Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA;
- Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA;
- Department of Biochemistry, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA;
- Bee Research Laboratory, BARC-E, USDA-Agricultural Research Service, Beltsville, Maryland 20705, USA;
- National Program Staff, USDA-Agricultural Research Service, Beltsville, Maryland 20705, USA;
- ARC Special Centre for the Molecular Genetics of Development, Visual Sciences, Research School of Biological Sciences, The Australian National University, Canberra, Australian Capital Territory 0200, Australia;
- Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Department of Computer Science, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Department of Cell and Structural Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Department of Animal Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Neuroscience Program, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Program in Ecology and Evolutionary Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Department of Chemistry, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA;
- Bee Power, L.P., 16484 CR 319, Lynn Grove Road, Navasota, Texas 77868, USA;
- Heinrich-Heine Universitaet Duesseldorf, Institut fuer Genetik, Universitaetsstrasse 1, 40225 Duesseldorf, Germany;
- European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117 Heidelberg, Germany;
- Max Delbr|[uuml]|ck Center for Molecular Medicine, Robert-Roessle-Strasse 10, 13125 BerlinBuch, Germany;
- Department of Animal Science, Texas A&M University, College Station, Texas 77843, USA;
- Department of Entomology, Texas A&M University, College Station, Texas 77843, USA;
- Department of Chemistry, University of Houston, Houston, Texas 77204, USA;
- Department of Biology, and Biochemistry, University of Houston, Houston, Texas 77204, USA;
- Departamento de Gen|[eacute]|tica, Faculdade de Medicina de Ribeir|[atilde]|o Preto, Universidade de S|[atilde]|o Paulo, Ribeir|[atilde]|o Preto 14049-900, Brazil;
- Departamento de Biologia Celular e Molecular e Bioagentes Patog|[ecirc]|nicos, Faculdade de Medicina de Ribeir|[atilde]|o Preto, Universidade de S|[atilde]|o Paulo, Ribeir|[atilde]|o Preto 14049-900, Brazil;
- Departamento de Biologia, Faculdade de Filosofia, Ci|[ecirc]|ncias e Letras de Ribeir|[atilde]|o Preto, Universidade de S|[atilde]|o Paulo, Ribeir|[atilde]|o Preto 14049-900, Brazil;
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907, USA;
- Department of Genetic Medicine and Development, University of Geneva Medical School CMU, 1 rue Michel-Servet, 1211 Geneva, Switzerland;
- School of Life Sciences, Arizona State University, PO Box 874501, Tempe, Arizona 85287-4501, USA;
- Instituto de Matem|[aacute]|tica e Estat|[iacute]|stica, Universidade de S|[atilde]|o Paulo, S|[atilde]|o Paulo, Brazil;
- Institut f|[uuml]|r Zoologie, Molekulare |[Ouml]|kologie, Martin-Luther-Universit|[auml]|t Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germany;
- Department of Entomology, University of Arizona, Tucson, Arizona 857210036, USA;
- Laboratory for Genome Exploration Research Group, RIKEN Genomic Sciences Center, Yokohama 230-0045, Japan;
- Institut f|[uuml]|r Medizinische Strahlenkunde und Zellforschung, Versbacher Strasse 5, 97078 W|[uuml]|rzburg, Germany;
- Laboratory of Developmental Physiology, Genomics and Proteomics, K.U. Leuven, Naamsestraat 59 B-3000 Leuven, Belgium;
- Laboratory for Evolution and Development, Biochemistry Department, University of Otago, PO Box 56, Dunedin, New Zealand;
- Zoology Department, University of Otago, PO Box 56, Dunedin, New Zealand;
- Department of Evolution, Systematics, and Ecology, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel;
- The Sudarsky Center for Computational Biology, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel;
- Department of Biological Chemistry, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel;
- Center for Functional and Comparative Insect Genomics, Department of Cell Biology and Comparative Zoology, Institute of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark;
- Department of Biology, New York University, New York, New York 10003, USA;
- Neurobiology, FB Biology/Chemistry/Pharmacy, Free University Berlin, Koenigin-Luise-Strasse 28/30, 14195 Berlin, Germany;
- MRC Functional Genetics Unit, Department of Physiology Anatomy and Genetics, Le Gros Clark Building, University of Oxford, South Parks Road, Oxford OX1 3QX, UK;
- The Picower Institute for Learning and Memory and the Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA;
- CSIRO Entomology, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia;
- Laboratory of Zoophysiology, University of Ghent, K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium;
- Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27109, USA;
- USDA-ARS-GMPRC, 1515 College Avenue, Manhattan, Kansas 66502, USA;
- Division of Biology, Ackert Hall, Kansas State University, Manhattan, Kansas 66506, USA;
- Department of Biochemistry, Kansas State University, Manhattan, Kansas 66506, USA;
- Department of Cellular Biology, University of Georgia, Athens, Georgia 30602, USA;
- School of Life Sciences, University of Nevada Las Vegas, 4505 Maryland Parkway, Box 454004, Las Vegas, Nevada 89154-4004, USA;
- Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan;
- Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya 464-8601, Japan;
- Laboratoire Evolution, G|[eacute]|nomes et Sp|[eacute]|ciation Centre National de la Recherche Scientifique, 91198 Gif-sur-Yvette, France;
- Fellowship for Interpretation of Genomes, 15W155 81st Street, Burr Ridge, Illinois 60527, USA;
- US National Institutes of Health, National Human Genome Research Institute, 31 Center Drive, Bethesda, Maryland 20892, USA;
- National Center for Biotechnology Information, National Library of Medicine, Department of Health and Human Services, 8600 Rockville Pike, Bethesda, Maryland 20894, USA;
- Centre de Biologie et de Gestion des Populations, Institut National de la Recherche Agronomique, 34988 Saint-G|[eacute]|ly-duFesc, France;
- Institute for Cellular and Molecular Biology and Section of Integrative Biology, University of Texas, Austin, Texas 78712, USA;
- Virginia Bioinformatics Institute 0477, Bioinformatics Facility, Washington Street, Virginia Tech, Blacksburg, Virginia 24061, USA;
- Division of Genetics, Genomics and Development, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA;
- Genomics Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA;
- The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK;
- Softberry Inc., 116 Radio Circle, Suite 400, Mount Kisco, New York 10549, USA;
- Penn Genomics Institute, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA;
- Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK;
- Honey Bee Unit, USDA-ARS, 2413 East highway 83, Number 213, Weslaco, Texas 78596, USA;
- Slovak Academy of Sciences, Dubravska cesta 21, 845 51 Bratislava 45, Slovakia;
- Depatment of Entomology, Cornell University, Ithaca 14853, New York, USA;
- Department of Molecular Biology and Genetics, Cornell University, Ithaca 14853, New York, USA;
- Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 02138, USA;
- Institut de Biologie Mol|[eacute]|culaire et Cellulaire, CNRS, 15 rue Ren|[eacute]| Descartes, 67084 Strasbourg Cedex, France;
- Ume|[aring]| Centre for Molecular Pathogenesis, By. 6L, Ume|[aring]| University, S-90187 Ume|[aring]|, Sweden;
- Department of Entomology and Plant Pathology, Oklahoma State University, 127 NRC, Stillwater, Oklahoma 74078, USA;
- National Institute of Livestock and Grassland Science, 3-1-1 Kannondai, Tsukuba, Ibaraki, 305-8517, Japan;
- School of Biological Sciences, University of Sydney, New South Wales 2006, Australia;
- BACPAC Resources, Children's Hospital Oakland Research Institute, Oakland, California 94609, USA;
- Laboratoire de Biom|[eacute]|trie et Biologie Evolutive, UMR 5558, CNRS, Univ. Lyon 1, 69622 Villeurbanne Cedex, France;
- Department of Entomology, W.M. Keck Center for Behavioral Biology, Gardner Hall, MC 7613, North Carolina State University, Raleigh, North Carolina 27695, USA;
- Department of Entomology, Washington State University, Pullman, Washington 99164, USA;
- Department of Ecology & Evolutionary Biology/Entomology, Haworth Hall, 1200 Sunnyside Avenue, University of Kansas, Lawrence, Kansas 66045, USA;
- Department of Ecology and Evolutionary Biology, University of California, Irvine, 321 Steinhaus Hall, Irvine, California 92697, USA;
- NASA Ames Genome Research Facility, Moffet Field, California 94035, USA;
- Systemix Institute, Cupertino, California 95014, USA;
- Departement d'informatique et de recherche operationnelle, Universite de Montreal, CP 6128 succ. Centre-Ville, Montreal, Quebec H3C 3J7, Canada;
- Vector Research, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK;
- Research Institute of Oncology, L'Hospitalet 08907, Catalonia, Spain;
- Institut National de la Recherche Agronomique and Universit|[eacute]| de Nice Sophia Antipolis, UMR 1112, Centre de Recherche de Sophia Antipolis, 06903 Sophia Antipolis, France
Abstract
Here we report the genome sequence of the honeybee Apis mellifera, a key model for social behaviour and essential to global ecology through pollination. Compared with other sequenced insect genomes, the A. mellifera genome has high A+T and CpG contents, lacks major transposon families, evolves more slowly, and is more similar to vertebrates for circadian rhythm, RNA interference and DNA methylation genes, among others. Furthermore, A. mellifera has fewer genes for innate immunity, detoxification enzymes, cuticle-forming proteins and gustatory receptors, more genes for odorant receptors, and novel genes for nectar and pollen utilization, consistent with its ecology and social organization. Compared to Drosophila, genes in early developmental pathways differ in Apis, whereas similarities exist for functions that differ markedly, such as sex determination, brain function and behaviour. Population genetics suggests a novel African origin for the species A. mellifera and insights into whether Africanized bees spread throughout the New World via hybridization or displacement.
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