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

doi:10.1126/science.aaa4788

Comparative Study

. 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

Karen M Kapheim¹, Hailin Pan², Cai Li³, Steven L Salzberg⁴, Daniela Puiu⁵, Tanja Magoc⁵, Hugh M Robertson⁶, Matthew E Hudson⁷, Aarti Venkat⁸, Brielle J Fischman⁹, Alvaro Hernandez¹⁰, Mark Yandell¹¹, Daniel Ence¹², Carson Holt¹¹, George D Yocum¹³, William P Kemp¹³, Jordi Bosch¹⁴, Robert M Waterhouse¹⁵, Evgeny M Zdobnov¹⁶, Eckart Stolle¹⁷, F Bernhard Kraus¹⁸, Sophie Helbing¹⁹, Robin F A Moritz²⁰, Karl M Glastad²¹, Brendan G Hunt²², Michael A D Goodisman²¹, Frank Hauser²³, Cornelis J P Grimmelikhuijzen²³, Daniel Guariz Pinheiro²⁴, Francis Morais Franco Nunes²⁵, Michelle Prioli Miranda Soares²⁶, Érica Donato Tanaka²⁷, Zilá Luz Paulino Simões²⁶, Klaus Hartfelder²⁸, Jay D Evans²⁹, Seth M Barribeau³⁰, Reed M Johnson³¹, Jonathan H Massey³², Bruce R Southey³³, Martin Hasselmann³⁴, Daniel Hamacher³⁴, Matthias Biewer³⁴, Clement F Kent³⁵, Amro Zayed³⁶, Charles Blatti 3rd³⁷, Saurabh Sinha³⁷, J Spencer Johnston³⁸, Shawn J Hanrahan³⁸, Sarah D Kocher³⁹, Jun Wang⁴⁰, Gene E Robinson⁴¹, Guojie Zhang⁴²

Affiliations

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.

PMID: 25977371
PMCID: PMC5471836
DOI: 10.1126/science.aaa4788

Comparative Study

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

Karen M Kapheim et al. Science. 2015.

. 2015 Jun 5;348(6239):1139-43.

doi: 10.1126/science.aaa4788. Epub 2015 May 14.

Authors

Affiliations

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.

PMID: 25977371
PMCID: PMC5471836
DOI: 10.1126/science.aaa4788

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.

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Figures

**Fig. 1. Phylogeny and divergence times (28) of bees selected for genome analysis**
We analyzed two independent origins of simple eusociality from a solitary ancestor, one each in Apidae (white circle 1) and Halictidae (white circle 2), and two independent elaborations of complex eusociality in honeybees (gray circle 1) and stingless bees (gray circle 2). Most bees mate once, but honeybees mate with multiple males. All bees eat pollen and nectar from flowering plants. Species names are colored according to degree of social complexity: blue: ancestrally solitary; green: facultative simple eusociality; orange: obligate simple eusociality; red: obligate complex eusociality. The social biology of *E. mexicana* is unknown, but is representative of the facultative simple eusocial life history (29). Numbers in each box are approximate colony size on a log scale. MRCA, most recent common ancestor; mya, millions of years ago.

**Fig. 2. Genomic signatures of evolutionary transitions from solitary to group life**
(A) Increasing social complexity is associated with increasing presence of cis-regulatory TFBSs in promoter regions. Each bar represents a TFBS for which presence correlates significantly with social complexity (blue: positive; red: negative). (B) Relationship between predicted numberof methylated genes and social complexity before and after (inset) phylogenetic correction (see text for statistics). (C) TFBS motifs showing a relationship between social complexity and evolutionary rate of coding and noncoding sequences in different lineages. Bar length indicates the number of significant correlations (blue: positive; red: negative) between each motif score and social complexity (from Table 1) among genes evolving faster (solid) or slower (hatched) in lineages with different levels of social complexity [from (D)]. Background shading follows circle shading in Fig. 1. (D) Number of genes for which evolutionary rate is faster or slower in lineages with higher compared to lower social complexity. Pie charts represent the proportion of genes evolving slower (light green) or faster (dark orange) with increased social complexity. Venn diagram shading follows circle shading in Fig. 1. (E) Complex eusocial species have a reduced proportion of repetitive DNA compared to other bees (see text for statistics). LTR, long terminal repeat; LINE, long interspersed element; SINE, short interspersed element; DNA, DNA transposon; LARD, large retrotransposon derivative; TRIM, terminal repeat retrotransposon in miniature; MITE, miniature inverted-repeat transposable element; TES, transposable elements.

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References

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1. Johnson BR, Linksvayer TA. Q Rev Biol. 2010;85:57–79. - PubMed

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[1] Maynard Smith J, Szathmáry E. The Major Transitions in Evolution. Oxford Univ. Press; Oxford, UK: 1995.

[2] Maynard Smith J, Szathmáry E. The Major Transitions in Evolution. Oxford Univ. Press; Oxford, UK: 1995.

[3] Michener CD. The Social Behavior of the Bees. Harvard Univ. Press; Cambridge, MA: 1974.

[4] Michener CD. The Social Behavior of the Bees. Harvard Univ. Press; Cambridge, MA: 1974.

[5] Klein AM, et al. Proc Biol Sci B. 2007;274:303–313. - PMC - PubMed

[6] Klein AM, et al. Proc Biol Sci B. 2007;274:303–313. - PMC - PubMed

[7] Hölldobler H, Wilson EO. The Superorganism: The Beauty, Elegance and Strangeness of Insect Societies. Norton; New York: 2009.

[8] Hölldobler H, Wilson EO. The Superorganism: The Beauty, Elegance and Strangeness of Insect Societies. Norton; New York: 2009.

[9] Johnson BR, Linksvayer TA. Q Rev Biol. 2010;85:57–79. - PubMed

[10] Johnson BR, Linksvayer TA. Q Rev Biol. 2010;85:57–79. - PubMed

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

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

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