title: Social evolution. Genomic signatures of evolutionary transitions from solitary to group living.
abstract: The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.
authors.affiliation: Carl R. WoeseInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Biology, Utah State University, Logan, UT 84322, USA. karen.kapheim@usu.edu wangj@genomics.org.cn generobi@illinois.edu zhanggj@genomics.org.cn.
authors.forename: Karen M
authors.initials: KM
authors.lastname: Kapheim
authors.affiliation: China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China.
authors.forename: Hailin
authors.initials: H
authors.lastname: Pan
authors.affiliation: China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, 1350, Denmark.
authors.forename: Cai
authors.initials: C
authors.lastname: Li
authors.affiliation: Departments of Biomedical Engineering, Computer Science, and Biostatistics, Johns Hopkins University, Baltimore, MD 21218, USA. Center for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
authors.forename: Steven L
authors.initials: SL
authors.lastname: Salzberg
authors.affiliation: Center for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
authors.forename: Daniela
authors.initials: D
authors.lastname: Puiu
authors.affiliation: Center for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
authors.forename: Tanja
authors.initials: T
authors.lastname: Magoc
authors.affiliation: Carl R. WoeseInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
authors.forename: Hugh M
authors.initials: HM
authors.lastname: Robertson
authors.affiliation: Carl R. WoeseInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
authors.forename: Matthew E
authors.initials: ME
authors.lastname: Hudson
authors.affiliation: Carl R. WoeseInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Human Genetics, University of Chicago, Chicago, IL 60637, USA.
authors.forename: Aarti
authors.initials: A
authors.lastname: Venkat
authors.affiliation: Carl R. WoeseInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Program in Ecology and Evolutionary Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Biology, Hobart and William Smith Colleges, Geneva, NY 14456, USA.
authors.forename: Brielle J
authors.initials: BJ
authors.lastname: Fischman
authors.affiliation: Roy J. Carver Biotechnology Center, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
authors.forename: Alvaro
authors.initials: A
authors.lastname: Hernandez
authors.affiliation: Department of Human Genetics, Eccles Institute of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA. USTAR Center for Genetic Discovery, University of Utah, Salt Lake City, UT 84112, USA.
authors.forename: Mark
authors.initials: M
authors.lastname: Yandell
authors.affiliation: Department of Human Genetics, Eccles Institute of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA.
authors.forename: Daniel
authors.initials: D
authors.lastname: Ence
authors.affiliation: Department of Human Genetics, Eccles Institute of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA. USTAR Center for Genetic Discovery, University of Utah, Salt Lake City, UT 84112, USA.
authors.forename: Carson
authors.initials: C
authors.lastname: Holt
authors.affiliation: U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS) Red River Valley Agricultural Research Center, Biosciences Research Laboratory, Fargo, ND 58102, USA.
authors.forename: George D
authors.initials: GD
authors.lastname: Yocum
authors.affiliation: U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS) Red River Valley Agricultural Research Center, Biosciences Research Laboratory, Fargo, ND 58102, USA.
authors.forename: William P
authors.initials: WP
authors.lastname: Kemp
authors.affiliation: Center for Ecological Research and Forestry Applications (CREAF), Universitat Autonoma de Barcelona, 08193 Bellaterra, Spain.
authors.forename: Jordi
authors.initials: J
authors.lastname: Bosch
authors.affiliation: Department of Genetic Medicine and Development, University of Geneva Medical School, 1211 Geneva, Switzerland. Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland. Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology (MIT), Cambridge, MA 02139, USA. The Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA.
authors.forename: Robert M
authors.initials: RM
authors.lastname: Waterhouse
authors.affiliation: Department of Genetic Medicine and Development, University of Geneva Medical School, 1211 Geneva, Switzerland. Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland.
authors.forename: Evgeny M
authors.initials: EM
authors.lastname: Zdobnov
authors.affiliation: Institute of Biology, Department Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germany. Queen Mary University of London, School of Biological and Chemical Sciences Organismal Biology Research Group, London E1 4NS, UK.
authors.forename: Eckart
authors.initials: E
authors.lastname: Stolle
authors.affiliation: Institute of Biology, Department Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germany. Department of Laboratory Medicine, University Hospital Halle, Ernst Grube Strasse 40, D-06120 Halle (Saale), Germany.
authors.forename: F Bernhard
authors.initials: FB
authors.lastname: Kraus
authors.affiliation: Institute of Biology, Department Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germany.
authors.forename: Sophie
authors.initials: S
authors.lastname: Helbing
authors.affiliation: Institute of Biology, Department Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germany. German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-Leipzig, 04103 Leipzig, Germany.
authors.forename: Robin F A
authors.initials: RF
authors.lastname: Moritz
authors.affiliation: School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.
authors.forename: Karl M
authors.initials: KM
authors.lastname: Glastad
authors.affiliation: Department of Entomology, University of Georgia, Griffin, GA 30223, USA.
authors.forename: Brendan G
authors.initials: BG
authors.lastname: Hunt
authors.affiliation: School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.
authors.forename: Michael A D
authors.initials: MA
authors.lastname: Goodisman
authors.affiliation: Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
authors.forename: Frank
authors.initials: F
authors.lastname: Hauser
authors.affiliation: Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
authors.forename: Cornelis J P
authors.initials: CJ
authors.lastname: Grimmelikhuijzen
authors.affiliation: Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901 Ribeirão Preto, SP, Brazil. Departamento de Tecnologia, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista (UNESP), 14884-900 Jaboticabal, SP, Brazil.
authors.forename: Daniel Guariz
authors.initials: DG
authors.lastname: Pinheiro
authors.affiliation: Departamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, 13565-905 São Carlos, SP, Brazil.
authors.forename: Francis Morais Franco
authors.initials: FM
authors.lastname: Nunes
authors.affiliation: Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901 Ribeirão Preto, SP, Brazil.
authors.forename: Michelle Prioli Miranda
authors.initials: MP
authors.lastname: Soares
authors.affiliation: Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, 14049-900 Ribeirão Preto, SP, Brazil.
authors.forename: Érica Donato
authors.initials: ÉD
authors.lastname: Tanaka
authors.affiliation: Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901 Ribeirão Preto, SP, Brazil.
authors.forename: Zilá Luz Paulino
authors.initials: ZL
authors.lastname: Simões
authors.affiliation: Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, 14049-900 Ribeirão Preto, SP, Brazil.
authors.forename: Klaus
authors.initials: K
authors.lastname: Hartfelder
authors.affiliation: USDA-ARS Bee Research Lab, Beltsville, MD 20705 USA.
authors.forename: Jay D
authors.initials: JD
authors.lastname: Evans
authors.affiliation: Department of Biology, East Carolina University, Greenville, NC 27858, USA.
authors.forename: Seth M
authors.initials: SM
authors.lastname: Barribeau
authors.affiliation: Department of Entomology, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH 44691, USA.
authors.forename: Reed M
authors.initials: RM
authors.lastname: Johnson
authors.affiliation: Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA.
authors.forename: Jonathan H
authors.initials: JH
authors.lastname: Massey
authors.affiliation: Department of Animal Sciences, University of Illinois, Urbana, IL 61801, USA.
authors.forename: Bruce R
authors.initials: BR
authors.lastname: Southey
authors.affiliation: Department of Population Genomics, Institute of Animal Husbandry and Animal Breeding, University of Hohenheim, Germany.
authors.forename: Martin
authors.initials: M
authors.lastname: Hasselmann
authors.affiliation: Department of Population Genomics, Institute of Animal Husbandry and Animal Breeding, University of Hohenheim, Germany.
authors.forename: Daniel
authors.initials: D
authors.lastname: Hamacher
authors.affiliation: Department of Population Genomics, Institute of Animal Husbandry and Animal Breeding, University of Hohenheim, Germany.
authors.forename: Matthias
authors.initials: M
authors.lastname: Biewer
authors.affiliation: Department of Biology, York University, Toronto, ON M3J 1P3, Canada. Janelia Farm Research Campus, Howard Hughes Medical Institue, Ashburn, VA 20147, USA.
authors.forename: Clement F
authors.initials: CF
authors.lastname: Kent
authors.affiliation: Department of Biology, York University, Toronto, ON M3J 1P3, Canada.
authors.forename: Amro
authors.initials: A
authors.lastname: Zayed
authors.affiliation: Carl R. WoeseInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Computer Science, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
authors.forename: Charles
authors.initials: C
authors.lastname: Blatti
authors.affiliation: Carl R. WoeseInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Department of Computer Science, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
authors.forename: Saurabh
authors.initials: S
authors.lastname: Sinha
authors.affiliation: Department of Entomology, Texas A&M University, College Station, TX 77843, USA.
authors.forename: J Spencer
authors.initials: JS
authors.lastname: Johnston
authors.affiliation: Department of Entomology, Texas A&M University, College Station, TX 77843, USA.
authors.forename: Shawn J
authors.initials: SJ
authors.lastname: Hanrahan
authors.affiliation: Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.
authors.forename: Sarah D
authors.initials: SD
authors.lastname: Kocher
authors.affiliation: China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China. Department of Biology, University of Copenhagen, 2200 Copenhagen, Denmark. Princess Al Jawhara Center of Excellence in the Research of Hereditary Disorders, King Abdulaziz University, Jeddah 21589, Saudi Arabia. Macau University of Science and Technology, Avenida Wai long, Taipa, Macau 999078, China. Department of Medicine, University of Hong Kong, Hong Kong. karen.kapheim@usu.edu wangj@genomics.org.cn generobi@illinois.edu zhanggj@genomics.org.cn.
authors.forename: Jun
authors.initials: J
authors.lastname: Wang
authors.affiliation: Carl R. WoeseInstitute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. Center for Advanced Study Professor in Entomology and Neuroscience, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. karen.kapheim@usu.edu wangj@genomics.org.cn generobi@illinois.edu zhanggj@genomics.org.cn.
authors.forename: Gene E
authors.initials: GE
authors.lastname: Robinson
authors.affiliation: China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China. Centre for Social Evolution, Department of Biology, Universitetsparken 15, University of Copenhagen, DK-2100 Copenhagen, Denmark. karen.kapheim@usu.edu wangj@genomics.org.cn generobi@illinois.edu zhanggj@genomics.org.cn.
authors.forename: Guojie
authors.initials: G
authors.lastname: Zhang
mesh_terms: D051046:Amino-Acid N-Acetyltransferase; D000818:Animals; D001516:Bees / Q000145:classification / Q000235:genetics*; D004251:DNA Transposable Elements; D019143:Evolution, Molecular; D005786:Gene Expression Regulation; D053263:Gene Regulatory Networks; D040961:Genetic Drift; D049750:Genome, Insect / Q000235:genetics; D010802:Phylogeny; D012641:Selection, Genetic; D012919:Social Behavior; D014157:Transcription Factors / Q000737:chemistry / Q000235:genetics; D059467:Transcriptome
chemical_list: D004251:DNA Transposable Elements; D014157:Transcription Factors; D051046:Amino-Acid N-Acetyltransferase