Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies
Edited by Joan E. Strassmann, Washington University in St. Louis, St. Louis, MO, and approved September 16, 2015 (received for review August 11, 2015)
Significance
In eusocial insect societies, such as ants and some bees and wasps, phenotypes are highly plastic, generating alternative phenotypes (queens and workers) from the same genome. The greatest plasticity is found in simple insect societies, in which individuals can switch between phenotypes as adults. The genomic, transcriptional, and epigenetic underpinnings of such plasticity are largely unknown. In contrast to the complex societies of the honeybee, we find that simple insect societies lack distinct transcriptional differentiation between phenotypes and coherently patterned DNA methylomes. Instead, alternative phenotypes are largely defined by subtle transcriptional network organization. These traits may facilitate genomic plasticity. These insights and resources will stimulate new approaches and hypotheses that will help to unravel the genomic processes that create phenotypic plasticity.
Abstract
Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.
Data Availability
Data deposition: Genomic analyses were performed on the whole-genome assemblies of Polistes canadensis and Dinoponera quadriceps, deposited at the DNA Data Bank of Japan/European Molecular Biology Laboratory/GenBank under the accession nos. PRJNA253269 and PRJNA253275, respectively. Raw data from all bisulfite-sequencing and RNA-sequencing libraries were deposited in the Gene Expression Omnibus (GEO) database (accession no. GSE59525).
Acknowledgments
We thank J. O. Dantas, A. Andrade, N. Dantas, R. Zaurin, E. Bell, R. Southon, W. T. Wcislo, J. Morales, and staff at the Galeta field station at the Smithsonian Tropical Research Institute Panama and the Universidade Federal de Sergipe for help and logistical support in fieldwork; D. Datta at the Centre for Genomic Regulation (CRG), K. Tabbada at the Babraham Institute, and N. Smerdon at The Wellcome Trust Sanger Institute for assistance with sequencing; T. Alioto of the Centro Nacional de Análisis Genómico in Barcelona for bioinformatics assistance; N. J. B. Isaac for statistical advice; groups that provided us with unpublished data (Dataset S3); and members of the W.R. and S.S. laboratories for their useful comments during the preparation of the manuscript. This work was conducted under Collecting and Export Permits SE/A-20-12, 10BR004553/DF, and 11BR006471/DF. This work was funded by Natural Environment Research Council Grants NE/G000638/1, NBAF581, and NE/K011316/1 (to S.S.) and Grant NE/G012121/1 (to W.O.H.H. and S.S.); the Research Councils UK (S.S); the Cancer Research UK Grant C14303/A17197 (to S.B); the Leverhulme Trust (W.O.H.H.); German Federal Ministry of Education and Research Grant FKZ 0315962 B; CRG core funding (to H.H.); Spanish Ministry of Economy and Competitiveness (MINECO) Grant BIO2012-37161 (to T.G.); MINECO Grant BIO2011-26205 (to R.G.); Instituto de Salud Carlos III Grant PT13/0001/0021 (to R.G.); the Instituto Nacional de Bioinformatica and Agència de Gestió d'Ajuts Universitaris i de Recerca (R.G.); Wellcome Trust Grants 095645/Z/11/Z (to W.R.) and WT099232 (to S.B); Biotechnology and Biological Sciences Research Council Grant BB/K010867/1 (to W.R.); the Stuttgart Universität (T.P.J.); and Fundaçao de Amparo à Pesquisa do Estado de Sao Paulo Grant 2010/10027-5 (to F.S.N.).
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Cover image: Pictured is an acute myeloblastic leukemic (AML) cancer cell penetrated by dendrites from a natural killer cell. The dendrites pump toxic material into the cell, just as a gasoline pump delivers fuel to a car. Kyungmoo Yea et al. used an agonist antibody to convert AML cells into natural killer cells. The authors found that the antibody targeted leukemic cells but not normal bone marrow cells, and that the differentiated natural killer cells attacked and killed undifferentiated leukemic cells. The results suggest that antibodies can be used to differentiate cancer cells into a phenotype that can attack malignant cells, according to the authors. See the article by Yea et al. on pages E6158–E6165. Image courtesy of Richard A. Lerner.
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Copyright
Freely available online through the PNAS open access option.
Data Availability
Data deposition: Genomic analyses were performed on the whole-genome assemblies of Polistes canadensis and Dinoponera quadriceps, deposited at the DNA Data Bank of Japan/European Molecular Biology Laboratory/GenBank under the accession nos. PRJNA253269 and PRJNA253275, respectively. Raw data from all bisulfite-sequencing and RNA-sequencing libraries were deposited in the Gene Expression Omnibus (GEO) database (accession no. GSE59525).
Submission history
Published online: October 19, 2015
Published in issue: November 10, 2015
Keywords
Acknowledgments
We thank J. O. Dantas, A. Andrade, N. Dantas, R. Zaurin, E. Bell, R. Southon, W. T. Wcislo, J. Morales, and staff at the Galeta field station at the Smithsonian Tropical Research Institute Panama and the Universidade Federal de Sergipe for help and logistical support in fieldwork; D. Datta at the Centre for Genomic Regulation (CRG), K. Tabbada at the Babraham Institute, and N. Smerdon at The Wellcome Trust Sanger Institute for assistance with sequencing; T. Alioto of the Centro Nacional de Análisis Genómico in Barcelona for bioinformatics assistance; N. J. B. Isaac for statistical advice; groups that provided us with unpublished data (Dataset S3); and members of the W.R. and S.S. laboratories for their useful comments during the preparation of the manuscript. This work was conducted under Collecting and Export Permits SE/A-20-12, 10BR004553/DF, and 11BR006471/DF. This work was funded by Natural Environment Research Council Grants NE/G000638/1, NBAF581, and NE/K011316/1 (to S.S.) and Grant NE/G012121/1 (to W.O.H.H. and S.S.); the Research Councils UK (S.S); the Cancer Research UK Grant C14303/A17197 (to S.B); the Leverhulme Trust (W.O.H.H.); German Federal Ministry of Education and Research Grant FKZ 0315962 B; CRG core funding (to H.H.); Spanish Ministry of Economy and Competitiveness (MINECO) Grant BIO2012-37161 (to T.G.); MINECO Grant BIO2011-26205 (to R.G.); Instituto de Salud Carlos III Grant PT13/0001/0021 (to R.G.); the Instituto Nacional de Bioinformatica and Agència de Gestió d'Ajuts Universitaris i de Recerca (R.G.); Wellcome Trust Grants 095645/Z/11/Z (to W.R.) and WT099232 (to S.B); Biotechnology and Biological Sciences Research Council Grant BB/K010867/1 (to W.R.); the Stuttgart Universität (T.P.J.); and Fundaçao de Amparo à Pesquisa do Estado de Sao Paulo Grant 2010/10027-5 (to F.S.N.).
Notes
This article is a PNAS Direct Submission.
See Commentary on page 13755.
Authors
Competing Interests
Conflict of interest statement: S.B. is a founder and shareholder of Cambridge Epigenetix Limited, and W.R. is a consultant and shareholder of Cambridge Epigenetix Limited.
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