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Genomic signatures of evolutionary transitions from solitary to group living
Abstract
For bees, many roads lead to social harmony: Eusociality, where workers sacrifice their reproductive rights to support the colony, has evolved repeatedly and represents the most evolved form of social evolution in insects. Kapheim et al. looked across the genomes of 10 bee species with varying degrees of sociality to determine the underlying genomic contributions. No one genomic path led to eusociality, but similarities across genomes were seen in features such as increases in gene regulation and methylation. It also seems that selection pressures relaxed after the emergence of complex sociality. Science , this issue p. 1139
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“The result from Kapheim et al. (88) gives the first glimpse of a special signature tied to GRNs for social behavior, but this is intriguingly reminiscent of a cis-regulatory signature seen in developmental studies in Drosophila.”
From Behavior-related gene regulatory networks: A new level of organization in the brain (2020) · cites this paper as [88]
In the citing paper
“These finding and those in refs. 89–91 support the prediction that changes in gene regulation are key features of the evolutionary transition from solitary to social life, at least in the social insects.”
From Behavior-related gene regulatory networks: A new level of organization in the brain (2020) · cites this paper as [88]
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“Kapheim et al. (88) bioinformatically detected greater TF binding site presence (reflecting stronger binding of TFs) in gene regulatory regions from social bees compared to orthologs from solitary bee species.”
From Behavior-related gene regulatory networks: A new level of organization in the brain (2020) · cites this paper as [88]
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“This result suggested that gene regulation in social bees has increased capacity and complexity relative to nonsocial bees, encoded in the DNA.”
From Behavior-related gene regulatory networks: A new level of organization in the brain (2020) · cites this paper as [88]
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Self-citationDNA methylation in social insects: how epigenetics can control behavior and longevity
Yan, H., Bonasio, R., Simola, D. F., Liebig, J., Berger, S. L., & Reinberg, D. (2015) · Annual Review of Entomology · doi:10.1146/annurev-ento-010814-020803 · Cited by 183
The bee tree of life: a supermatrix approach to apoid phylogeny and biogeography
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Cloning and identification of an oxytocin/vasopressin-like receptor and its ligand from insects
Stafflinger, E., Hansen, K. K., Hauser, F., Schneider, M., Cazzamali, G., Williamson, M. P., & Grimmelikhuijzen, C. J. P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710897105 · Cited by 180
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Self-citationRelaxed selection is a precursor to the evolution of phenotypic plasticity
Hunt, B. G., Ometto, L., Wurm, Y., Shoemaker, D., Yi, S. V., Keller, L., & Goodisman, M. A. D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104825108 · Cited by 175
Self-citationOrthoDB: the hierarchical catalog of eukaryotic orthologs
Kriventseva, E. V., Rahman, N., Espinosa, O., & Zdobnov, E. M. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm845 · Cited by 170
Self-citationMuñoz-Torres, M. C., Reese, J., Childers, C. P., Bennett, A. K., Sundaram, J. P., Childs, K. L., Anzola, J. M., Milshina, N. V., & Elsik, C. G. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1145 · Cited by 166
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Sex Determination in Insects: Variations on a Common Theme
Bopp, D., Saccone, G., & Beye, M. (2013) · Sexual Development · doi:10.1159/000356458 · Cited by 161
Yang, T., & Liu, N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029418 · Cited by 151
Deconstructing the Superorganism: Social Physiology, Groundplans, and Sociogenomics
Johnson, B. R., & Linksvayer, T. A. (2010) · The Quarterly Review of Biology · doi:10.1086/650290 · Cited by 150
Patterns of Positive Selection in Seven Ant Genomes
Roux, J., Privman, E., Moretti, S., Daub, J. T., Robinson‐Rechavi, M., & Keller, L. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu141 · Cited by 147
The Effects of Recombination Rate on the Distribution and Abundance of Transposable Elements
Dolgin, E., & Charlesworth, B. (2008) · Genetics · doi:10.1534/genetics.107.082743 · Cited by 145
Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae)
Mao, W., Rupasinghe, S. G., Johnson, R. M., Zangerl, A. R., Schuler, M. A., & Berenbaum, M. R. (2009) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2009.08.008 · Cited by 140
Self-citationOrthoDB: the hierarchical catalog of eukaryotic orthologs in 2011
Waterhouse, R. M., Zdobnov, E. M., Tegenfeldt, F., Li, J., & Kriventseva, E. V. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq930 · Cited by 140
Self-citationPheromone anosmia in a scarab beetle induced by in vivo inhibition of a pheromone-degrading enzyme
Maı̈bèche, M., Nikonov, A. A., Ishida, Y., Jacquin‐Joly, E., & Leal, W. S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403537101 · Cited by 137
Kapitonov, V. V., Tempel, S., & Jurka, J. (2009) · Gene · doi:10.1016/j.gene.2009.07.019 · Cited by 129
Phenotypic connections in surprising places
Linghu, B., & DeLisi, C. (2010) · Genome biology · doi:10.1186/gb-2010-11-4-116 · Cited by 128
Feldmeyer, B., Elsner, D., & Foitzik, S. (2013) · Molecular Ecology · doi:10.1111/mec.12490 · Cited by 120
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Self-citationWNTs in synapse formation and neuronal circuitry
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Methylation and worker reproduction in the bumble-bee (Bombus terrestris)
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Self-citationPopulation genomics of eusocial insects: the costs of a vertebrate‐like effective population size
Romiguier, J., Lourenco, J., Gayral, P., Faivre, N., Weinert, L. A., Ravel, S., Ballenghien, M., Cahais, V., Bernard, A., Loire, É., et al. (2014) · Journal of Evolutionary Biology · doi:10.1111/jeb.12331 · Cited by 105
The Function of Intragenic DNA Methylation: Insights from Insect Epigenomes
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The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes
Kocher, S. D., Li, C., Yang, W. C., Tan, H., Yi, S. V., Yang, X., Hoekstra, H. E., Zhang, G., Pierce, N. E., & Yu, D. W. (2013) · Genome biology · doi:10.1186/gb-2013-14-12-r142 · Cited by 84
Self-citationMultiple Mariner Transposons in Flatworms and Hydras Are Related to Those of Insects
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Self-citationDiscovery of Defense- and Neuropeptides in Social Ants by Genome-Mining
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DNA methylation changes elicited by social stimuli in the brains of worker honey bees
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Self-citationHorizontal transfers of Mariner transposons between mammals and insects
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Self-citationDifferential expression of hypoxia pathway genes in honey bee (Apis mellifera L.) caste development
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Self-citation
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Cited by
Convergent evolution in the genomics era: new insights and directions
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Reciprocity and alignment: quantifying coupling in dynamic interactions
Dumas, G., & Fairhurst, M. T. (2021) · Royal Society Open Science · doi:10.1098/rsos.210138 · Cited by 88
Behavior-related gene regulatory networks: A new level of organization in the brain
Sinha, S., Jones, B. M., Traniello, I. M., Bukhari, S. A., Halfon, M. S., Hofmann, H. A., Huang, S., Katz, P. S., Keagy, J., Lynch, V. J., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921625117 · Cited by 85
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The Birth-and-Death Evolution of Cytochrome P450 Genes in Bees
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Metadata
- Authors
- Kapheim, K. M., Pan, H., Li, C., Salzberg, S. L., Puiu, D., Magoc, T., Robertson, H. M., Hudson, M. E., Venkat, A., Fischman, B. J., Hernandez, A., Yandell, M., Ence, D., Holt, C., Yocum, G. D., Kemp, W. P., Bosch, J., Waterhouse, R. M., Zdobnov, E. M., Stolle, E., Kraus, F. B., Helbing, S., Moritz, R. F. A., Glastad, K. M., Hunt, B. G., Goodisman, M. A. D., Hauser, F., Grimmelikhuijzen, C. J. P., Pinheiro, D. G., Nunes, F. M. F., Soares, M. P. M., Tanaka, É. D., Simões, Z. L. P., Hartfelder, K., Evans, J. D., Barribeau, S. M., Johnson, R. M., Massey, J. H., Southey, B. R., Hasselmann, M., Hamacher, D., Biewer, M., Kent, C. F., Zayed, A., Blatti, C., Sinha, S., Johnston, J. S., Hanrahan, S. J., Kocher, S. D., Wang, J., Robinson, G. E., & Zhang, G.
- Affiliations
- Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
- China National GeneBank, BGI-Shenzhen, Shenzhen, 518083, China.
- 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.
- Roy J. Carver Biotechnology Center, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
- Department of Human Genetics, Eccles Institute of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA.
- U.S. Department of Agriculture–Agricultural Research Service (USDA-ARS) Red River Valley Agricultural Research Center, Biosciences Research Laboratory, Fargo, ND 58102, USA.
- Center for Ecological Research and Forestry Applications (CREAF), Universitat Autonoma de Barcelona, 08193 Bellaterra, Spain.
- Department of Genetic Medicine and Development, University of Geneva Medical School, 1211 Geneva, Switzerland.
- Institute of Biology, Department Zoology, Martin-Luther-University Halle-Wittenberg, Hoher Weg 4, D-06099 Halle (Saale), Germany.
- School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.
- Department of Entomology, University of Georgia, Griffin, GA 30223, USA.
- Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, Copenhagen, Denmark.
- Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901 Ribeirão Preto, SP, Brazil.
- Departamento de Genética e Evolução, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos, 13565-905 São Carlos, SP, Brazil.
- Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, 14049-900 Ribeirão Preto, SP, Brazil.
- 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.
- USDA-ARS Bee Research Lab, Beltsville, MD 20705 USA.
- Department of Biology, East Carolina University, Greenville, NC 27858, USA.
- Department of Entomology, Ohio Agricultural Research and Development Center, Ohio State University, Wooster, OH 44691, USA.
- Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
- Department of Animal Sciences, University of Illinois, Urbana, IL 61801, USA.
- Department of Population Genomics, Institute of Animal Husbandry and Animal Breeding, University of Hohenheim, Germany.
- Department of Biology, York University, Toronto, ON M3J 1P3, Canada.
- Department of Entomology, Texas A&M University, College Station, TX 77843, USA.
- Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA.
- Venue
- Science
- Published
- 2015-06-05
- Volume
- 348
- Issue
- 6239
- Pages
- 1139-1143
- ISSN
- 0036-8075
- 1095-9203
- PMC
- PMC5471836
- Cited by
- 409
- References
- 149
- Language
- en
- Funders
- U.S. National Science Foundation (DEB-0640690, DEB-0743154)
- Natural Sciences and Engineering Research Council of Canada
- Swiss National Science Foundation (31003A-125350)
- BGI
- Lundbeck Foundation
- Danish Council for Independent Research (10-081390, 0602-01170B)
- U.S. National Institutes of Health Pioneer Award (DP1 OD006416)
- European Union Marie Curie International Incoming Fellowship (300837)
- Georgia Tech-Elizabeth Smithgall Watts
- Marie Curie International Outgoing Fellowship (PIOF-GA-2011-303312)
- Commission Informatique of the University of Geneva
- Schmidheiny Foundation
- Swiss Institute of Bioinformatics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.