title: The genomes of two key bumblebee species with primitive eusocial organization.
abstract: BACKGROUND
  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.
  
  
  RESULTS
  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.
  
  
  CONCLUSIONS
  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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authors.affiliation: School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA. f.wolschin@gmail.com.|Department of Chemistry, Biotechnology and Food Science, Norwegian University of Food Science, N-1432, Aas, Norway. f.wolschin@gmail.com.
authors.forename: Florian
authors.initials: F
authors.lastname: Wolschin
authors.affiliation: Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium. na.yu@ugent.be.
authors.forename: Na
authors.initials: N
authors.lastname: Yu
authors.affiliation: Department of Genetic Medicine and Development, University of Geneva Medical School, rue Michel-Servet 1, 1211, Geneva, Switzerland. Evgeny.Zdobnov@unige.ch.|Swiss Institute of Bioinformatics, rue Michel-Servet 1, 1211, Geneva, Switzerland. Evgeny.Zdobnov@unige.ch.
authors.forename: Evgeny M
authors.initials: EM
authors.lastname: Zdobnov
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. uhpesh@gmail.com.
authors.forename: Peshtewani K
authors.initials: PK
authors.lastname: Aqrawi
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. kerstinb@bcm.edu.
authors.forename: Kerstin P
authors.initials: KP
authors.lastname: Blankenburg
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. mcoyle@bcm.edu.
authors.forename: Marcus
authors.initials: M
authors.lastname: Coyle
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. franciscol@livemail.uthscsa.edu.
authors.forename: Liezl
authors.initials: L
authors.lastname: Francisco
authors.affiliation: Roy J. Carver Biotechnology Center, University of Illinois Urbana-Champaign, Urbana, IL, USA. aghernan@illinois.edu.
authors.forename: Alvaro G
authors.initials: AG
authors.lastname: Hernandez
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. mholder@bcm.edu.
authors.forename: Michael
authors.initials: M
authors.lastname: Holder
authors.affiliation: Department of Crop Sciences and Institute of Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA. mhudson@illinois.edu.
authors.forename: Matthew E
authors.initials: ME
authors.lastname: Hudson
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. larondaj@bcm.edu.
authors.forename: LaRonda
authors.initials: L
authors.lastname: Jackson
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. jayaseel@bcm.edu.
authors.forename: Joy
authors.initials: J
authors.lastname: Jayaseelan
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. vanditajoshi@gmail.com.
authors.forename: Vandita
authors.initials: V
authors.lastname: Joshi
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. ckovar@bcm.edu.
authors.forename: Christie
authors.initials: C
authors.lastname: Kovar
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. sllee@bcm.edu.
authors.forename: Sandra L
authors.initials: SL
authors.lastname: Lee
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. Robert.mata.jr@gmail.com.
authors.forename: Robert
authors.initials: R
authors.lastname: Mata
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. Tittu.Mathew@bcm.edu.
authors.forename: Tittu
authors.initials: T
authors.lastname: Mathew
authors.affiliation: Molecular Genetic Technology Program, School of Health Professions, MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 2, Houston, TX, 77025, USA. inewsham@mdanderson.org.
authors.forename: Irene F
authors.initials: IF
authors.lastname: Newsham
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. bearrnn@hotmail.com.
authors.forename: Robin
authors.initials: R
authors.lastname: Ngo
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. gokwuonu@bcm.edu.
authors.forename: Geoffrey
authors.initials: G
authors.lastname: Okwuonu
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. c.duy.pham@gmail.com.
authors.forename: Christopher
authors.initials: C
authors.lastname: Pham
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. lpu1562633518@gmail.com.
authors.forename: Ling-Ling
authors.initials: LL
authors.lastname: Pu
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. nehads@bcm.edu.
authors.forename: Nehad
authors.initials: N
authors.lastname: Saada
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. jirehs@bcm.edu.
authors.forename: Jireh
authors.initials: J
authors.lastname: Santibanez
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. DeNard.Simmons@utsa.edu.
authors.forename: DeNard
authors.initials: D
authors.lastname: Simmons
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. rthornto@bcm.edu.
authors.forename: Rebecca
authors.initials: R
authors.lastname: Thornton
authors.affiliation: Department of Human Genetics, University of Chicago, Chicago, IL, USA. aartiv@uchicago.edu.
authors.forename: Aarti
authors.initials: A
authors.lastname: Venkat
authors.affiliation: Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA. k-walden@life.illinois.edu.
authors.forename: Kimberly K O
authors.initials: KK
authors.lastname: Walden
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. ywu@mdanderson.org.
authors.forename: Yuan-Qing
authors.initials: YQ
authors.lastname: Wu
authors.affiliation: Laboratory of Protein Biochemistry and Biomolecular Engineering, Department of Biochemistry and Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium. Griet.Debyser@UGent.be.
authors.forename: Griet
authors.initials: G
authors.lastname: Debyser
authors.affiliation: Laboratory of Protein Biochemistry and Biomolecular Engineering, Department of Biochemistry and Microbiology, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium. Bart.Devreese@UGent.be.
authors.forename: Bart
authors.initials: B
authors.lastname: Devreese
authors.affiliation: Institute of Zoology, Zoological Society of London, Regent's Park, London, NW1 4RY, UK. Claireasher13@gmail.com.
authors.forename: Claire
authors.initials: C
authors.lastname: Asher
authors.affiliation: 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. julie.blommaert@xtra.co.nz.
authors.forename: Julie
authors.initials: J
authors.lastname: Blommaert
authors.affiliation: Department of Ecology, Evolution, and Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel. ariel.chipman@mail.huji.ac.il.
authors.forename: Ariel D
authors.initials: AD
authors.lastname: Chipman
authors.affiliation: Department of Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK. l.chittka@qmul.ac.uk.
authors.forename: Lars
authors.initials: L
authors.lastname: Chittka
authors.affiliation: Institute of Biology, Martin-Luther-University Halle-Wittenberg, Wittenberg, Germany. bertrand.fouks@zoologie.uni-halle.de.|Department of Biology, University of North Carolina at Greensboro, 321 McIver Street, Greensboro, NC, 27403, USA. bertrand.fouks@zoologie.uni-halle.de.
authors.forename: Bertrand
authors.initials: B
authors.lastname: Fouks
authors.affiliation: Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium. jasonleu.jisheng.liu@gmail.com.|School of Life Sciences, Guangzhou University, Guangzhou, China. jasonleu.jisheng.liu@gmail.com.
authors.forename: Jisheng
authors.initials: J
authors.lastname: Liu
authors.affiliation: 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. meaghan.p.oneill@gmail.com.
authors.forename: Meaghan P
authors.initials: MP
authors.lastname: O'Neill
authors.affiliation: School of Biological Sciences, University of Bristol, 24 Tyndall Avenue, Bristol, BS8 1TQ, UK. Seirian.Sumner@Bristol.ac.uk.
authors.forename: Seirian
authors.initials: S
authors.lastname: Sumner
authors.affiliation: Center for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA. dpuiu@jhu.edu.
authors.forename: Daniela
authors.initials: D
authors.lastname: Puiu
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. jiaxinqu@yahoo.com.
authors.forename: Jiaxin
authors.initials: J
authors.lastname: Qu
authors.affiliation: Center for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA. salzberg@jhu.edu.
authors.forename: Steven L
authors.initials: SL
authors.lastname: Salzberg
authors.affiliation: School of Life Sciences, Guangzhou University, Guangzhou, China. sscherer@bcm.edu.
authors.forename: Steven E
authors.initials: SE
authors.lastname: Scherer
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. donnam@bcm.edu.
authors.forename: Donna M
authors.initials: DM
authors.lastname: Muzny
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. stephenr@bcm.edu.
authors.forename: Stephen
authors.initials: S
authors.lastname: Richards
authors.affiliation: 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. generobi@illinois.edu.
authors.forename: Gene E
authors.initials: GE
authors.lastname: Robinson
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. agibbs@bcm.edu.
authors.forename: Richard A
authors.initials: RA
authors.lastname: Gibbs
authors.affiliation: Experimental Ecology, Institute of Integrative Biology, Eidgenössiche Technische Hochschule (ETH) Zürich, CH-8092, Zürich, Switzerland. psh@env.ethz.ch.
authors.forename: Paul
authors.initials: P
authors.lastname: Schmid-Hempel
authors.affiliation: Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, MS BCM226, One Baylor Plaza, Houston, TX, 77030, USA. kworley@bcm.edu.
authors.forename: Kim C
authors.initials: KC
authors.lastname: Worley
mesh_terms: D000818:Animals; D001514:Bee Venoms / Q000235:genetics; D001516:Bees / Q000145:classification / Q000235:genetics* / Q000502:physiology; D001522:Behavior, Animal; D002628:Chemoreceptor Cells / Q000378:metabolism; D002874:Chromosome Mapping; D030541:Databases, Genetic; D019143:Evolution, Molecular; D005260:Female; D005786:Gene Expression Regulation; D015321:Gene Rearrangement; D017344:Genes, Insect; D023281:Genomics; D020071:Interspersed Repetitive Sequences; D008297:Male; D016366:Open Reading Frames; D020641:Polymorphism, Single Nucleotide; D051140:Selenoproteins / Q000235:genetics / Q000378:metabolism; D017422:Sequence Analysis, DNA; D012919:Social Behavior; D013045:Species Specificity; D026801:Synteny
chemical_list: D001514:Bee Venoms; D051140:Selenoproteins