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Science. 2015 Jun 5;348(6239):1139-43. doi: 10.1126/science.aaa4788. Epub 2015 May 14.

Social evolution. Genomic signatures of evolutionary transitions from solitary to group living.

Author information

1
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.
2
China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China.
3
China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, 1350, Denmark.
4
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.
5
Center for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
6
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.
7
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.
8
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.
9
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.
10
Roy J. Carver Biotechnology Center, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
11
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.
12
Department of Human Genetics, Eccles Institute of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA.
13
U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS) Red River Valley Agricultural Research Center, Biosciences Research Laboratory, Fargo, ND 58102, USA.
14
Center for Ecological Research and Forestry Applications (CREAF), Universitat Autonoma de Barcelona, 08193 Bellaterra, Spain.
15
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.
16
Department of Genetic Medicine and Development, University of Geneva Medical School, 1211 Geneva, Switzerland. Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland.
17
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.
18
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.
19
Institute of Biology, Department Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germany.
20
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.
21
School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.
22
Department of Entomology, University of Georgia, Griffin, GA 30223, USA.
23
Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
24
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.
25
Departamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, 13565-905 São Carlos, SP, Brazil.
26
Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901 Ribeirão Preto, SP, Brazil.
27
Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, 14049-900 Ribeirão Preto, SP, Brazil.
28
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.
29
USDA-ARS Bee Research Lab, Beltsville, MD 20705 USA.
30
Department of Biology, East Carolina University, Greenville, NC 27858, USA.
31
Department of Entomology, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH 44691, USA.
32
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.
33
Department of Animal Sciences, University of Illinois, Urbana, IL 61801, USA.
34
Department of Population Genomics, Institute of Animal Husbandry and Animal Breeding, University of Hohenheim, Germany.
35
Department of Biology, York University, Toronto, ON M3J 1P3, Canada. Janelia Farm Research Campus, Howard Hughes Medical Institue, Ashburn, VA 20147, USA.
36
Department of Biology, York University, Toronto, ON M3J 1P3, Canada.
37
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.
38
Department of Entomology, Texas A&M University, College Station, TX 77843, USA.
39
Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.
40
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.
41
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.
42
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.

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.

PMID:
25977371
PMCID:
PMC5471836
DOI:
10.1126/science.aaa4788
[Indexed for MEDLINE]
Free PMC Article

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