Evidence map›Paper›PMID 25977371›Full record

ArticleScience (New York, N.Y.)2015

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

Karen M Kapheim, Hailin Pan, Cai Li, Steven L Salzberg, Daniela Puiu, Tanja Magoc, Hugh M Robertson, Matthew E Hudson, Aarti Venkat, Brielle J Fischman and 42 more

Abstract readComparative Study
In one paragraph

Article in Science (New York, N.Y.), 2015. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 176 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
176citing papers in PubMed, 1 pooled it
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

176 citing papers in PubMed, 1 synthesis or guideline pooled it.

  1. Pooled it
  2. Genome Evolution in Social Insects.Genome biology and evolution · 2026
    Review
  3. Article
  4. Article
  5. Article
  6. Article
  7. Article
  8. Review
  9. Article
  10. Article
  11. Article
  12. Fraternal cooperation of hierarchical cancer parallels metazoan multicellularity and eusociality.Biological reviews of the Cambridge Philosophical Society · 2026
    Review
  13. Review
  14. Article
  15. Article
  16. Article
  17. The Evolution of Bees: Insights from 'Omic Studies.Genome biology and evolution · 2026
    Review
  18. Article
  19. Article
  20. Article

116 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

52 authors.

Karen M KapheimCarl 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.
Hailin PanChina National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China.
Cai LiChina National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China. Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, 1350, Denmark.
Steven L SalzbergDepartments 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.
Daniela PuiuCenter for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Tanja MagocCenter for Computational Biology, McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Hugh M RobertsonCarl 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.
Matthew E HudsonCarl 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.
Aarti VenkatCarl 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.
Brielle J FischmanCarl 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.
Alvaro HernandezRoy J. Carver Biotechnology Center, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
Mark YandellDepartment 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.
Daniel EnceDepartment of Human Genetics, Eccles Institute of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA.
Carson HoltDepartment 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.
George D YocumU.S. Department of Agriculture-Agricultural Research Service (USDA-ARS) Red River Valley Agricultural Research Center, Biosciences Research Laboratory, Fargo, ND 58102, USA.
William P KempU.S. Department of Agriculture-Agricultural Research Service (USDA-ARS) Red River Valley Agricultural Research Center, Biosciences Research Laboratory, Fargo, ND 58102, USA.
Jordi BoschCenter for Ecological Research and Forestry Applications (CREAF), Universitat Autonoma de Barcelona, 08193 Bellaterra, Spain.
Robert M WaterhouseDepartment 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.
Evgeny M ZdobnovDepartment of Genetic Medicine and Development, University of Geneva Medical School, 1211 Geneva, Switzerland. Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland.
Eckart StolleInstitute 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.
F Bernhard KrausInstitute 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.
Sophie HelbingInstitute of Biology, Department Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germany.
Robin F A MoritzInstitute 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.
Karl M GlastadSchool of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.
Brendan G HuntDepartment of Entomology, University of Georgia, Griffin, GA 30223, USA.
Michael A D GoodismanSchool of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.
Frank HauserCenter for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
Cornelis J P GrimmelikhuijzenCenter for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
Daniel Guariz PinheiroDepartamento 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.
Francis Morais Franco NunesDepartamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, 13565-905 São Carlos, SP, Brazil.
Michelle Prioli Miranda SoaresDepartamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901 Ribeirão Preto, SP, Brazil.
Érica Donato TanakaDepartamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, 14049-900 Ribeirão Preto, SP, Brazil.
Zilá Luz Paulino SimõesDepartamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901 Ribeirão Preto, SP, Brazil.
Klaus HartfelderDepartamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, 14049-900 Ribeirão Preto, SP, Brazil.
Jay D EvansUSDA-ARS Bee Research Lab, Beltsville, MD 20705 USA.
Seth M BarribeauDepartment of Biology, East Carolina University, Greenville, NC 27858, USA.
Reed M JohnsonDepartment of Entomology, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH 44691, USA.
Jonathan H MasseyDepartment 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.
Bruce R SoutheyDepartment of Animal Sciences, University of Illinois, Urbana, IL 61801, USA.
Martin HasselmannDepartment of Population Genomics, Institute of Animal Husbandry and Animal Breeding, University of Hohenheim, Germany.
Daniel HamacherDepartment of Population Genomics, Institute of Animal Husbandry and Animal Breeding, University of Hohenheim, Germany.
Matthias BiewerDepartment of Population Genomics, Institute of Animal Husbandry and Animal Breeding, University of Hohenheim, Germany.
Clement F KentDepartment of Biology, York University, Toronto, ON M3J 1P3, Canada. Janelia Farm Research Campus, Howard Hughes Medical Institue, Ashburn, VA 20147, USA.
Amro ZayedDepartment of Biology, York University, Toronto, ON M3J 1P3, Canada.
Charles BlattiCarl 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.
Saurabh SinhaCarl 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.
J Spencer JohnstonDepartment of Entomology, Texas A&M University, College Station, TX 77843, USA.
Shawn J HanrahanDepartment of Entomology, Texas A&M University, College Station, TX 77843, USA.
Sarah D KocherDepartment of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.
Jun WangChina 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.
Gene E RobinsonCarl 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.
Guojie ZhangChina 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.

Funding

Johnny Bee Good: Bees as Models to Study the Hijacking of the Reward SystemDP1OD006416 · OD · UNIVERSITY OF ILLINOIS AT URBANA-CHAMPAIGN · PI ROBINSON, GENE E · 2009 to 2011
$2.4M
Howard Hughes Medical InstituteNIH HHS DP1 OD006416
6 · The paper itself

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.

Indexed as

Evolution, MolecularGenetic DriftSocial BehaviorTranscriptomeAmino-Acid N-AcetyltransferaseAnimalsBeesDNA Transposable ElementsGene Expression RegulationGene Regulatory NetworksGenome, InsectPhylogenySelection, GeneticTranscription FactorsAmino-Acid N-AcetyltransferaseDNA Transposable ElementsTranscription Factors

Identifiers

PMID25977371
PMCPMC5471836

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.