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Research Article

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Solenn Patalano, Anna Vlasova, Chris Wyatt, Philip Ewels, Francisco Camara, Pedro G. Ferreira, Claire L. Asher, Tomasz P. Jurkowski, Anne Segonds-Pichon, View ORCID ProfileMartin Bachman, Irene González-Navarrete, André E. Minoche, Felix Krueger, Ernesto Lowy, Marina Marcet-Houben, Jose Luis Rodriguez-Ales, Fabio S. Nascimento, Shankar Balasubramanian, Toni Gabaldon, James E. Tarver, Simon Andrews, Heinz Himmelbauer, William O. H. Hughes, Roderic Guigó, Wolf Reik, and Seirian Sumner
  1. aThe Babraham Institute, Cambridge CB22 3AT, United Kingdom;
  2. bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
  3. cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
  4. dSchool of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
  5. eDepartment of Biochemistry and Biophysics, Science for Life Laboratory, Stockholm University, Stockholm 106 91, Sweden;
  6. fInstituto de Investigação e Inovação em Saúde, Universidade do Porto, 4200-135 Porto, Portugal;
  7. gInstitute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), Institute of Molecular Pathology and Immunology, University of Porto, 4200-135 Porto, Portugal;
  8. hInstitute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom;
  9. iInstitute of Integrative and Comparative Biology, School of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom;
  10. jInstitute of Biochemistry, University of Stuttgart, 70569 Stuttgart, Germany;
  11. kDepartment of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom;
  12. lCancer Research UK Cambridge Institute, University of Cambridge, Cambridge CB2 ORE, United Kingdom;
  13. mMax Planck Institute for Molecular Genetics, 14195 Berlin, Germany;
  14. nDepartamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP)-Universidade de São Paulo, 14040-901, Ribeirão Preto-SP, Brazil;
  15. oSchool of Clinical Medicine, University of Cambridge, CB2 0SP, Cambridge, United Kingdom;
  16. pInstitució Catalana de Recerca i Estudis Avançats, 08010 Barcelona, Spain;
  17. qSchool of Earth Sciences, University of Bristol, BS8 1TQ, United Kingdom;
  18. rDepartment of Biotechnology, Universität für Bodenkultur, 1190 Vienna, Austria;
  19. sSchool of Life Sciences, University of Sussex, Brighton BN1 9QG, United Kingdom;
  20. tCentre for Trophoblast Research, University of Cambridge, Cambridge CB2 3EG, United Kingdom;
  21. uWellcome Trust Sanger Institute, Hinxton CB10 1SA, United Kingdom

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PNAS November 10, 2015 112 (45) 13970-13975; first published October 19, 2015; https://doi.org/10.1073/pnas.1515937112
Solenn Patalano
aThe Babraham Institute, Cambridge CB22 3AT, United Kingdom;
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  • For correspondence: solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk
Anna Vlasova
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
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Chris Wyatt
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
dSchool of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
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Philip Ewels
aThe Babraham Institute, Cambridge CB22 3AT, United Kingdom;
eDepartment of Biochemistry and Biophysics, Science for Life Laboratory, Stockholm University, Stockholm 106 91, Sweden;
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Francisco Camara
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
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Pedro G. Ferreira
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
fInstituto de Investigação e Inovação em Saúde, Universidade do Porto, 4200-135 Porto, Portugal;
gInstitute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), Institute of Molecular Pathology and Immunology, University of Porto, 4200-135 Porto, Portugal;
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Claire L. Asher
hInstitute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom;
iInstitute of Integrative and Comparative Biology, School of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom;
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Tomasz P. Jurkowski
jInstitute of Biochemistry, University of Stuttgart, 70569 Stuttgart, Germany;
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Anne Segonds-Pichon
aThe Babraham Institute, Cambridge CB22 3AT, United Kingdom;
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Martin Bachman
kDepartment of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom;
lCancer Research UK Cambridge Institute, University of Cambridge, Cambridge CB2 ORE, United Kingdom;
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  • ORCID record for Martin Bachman
Irene González-Navarrete
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
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André E. Minoche
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
mMax Planck Institute for Molecular Genetics, 14195 Berlin, Germany;
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Felix Krueger
aThe Babraham Institute, Cambridge CB22 3AT, United Kingdom;
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Ernesto Lowy
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
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Marina Marcet-Houben
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
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Jose Luis Rodriguez-Ales
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
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Fabio S. Nascimento
nDepartamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP)-Universidade de São Paulo, 14040-901, Ribeirão Preto-SP, Brazil;
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Shankar Balasubramanian
kDepartment of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom;
lCancer Research UK Cambridge Institute, University of Cambridge, Cambridge CB2 ORE, United Kingdom;
oSchool of Clinical Medicine, University of Cambridge, CB2 0SP, Cambridge, United Kingdom;
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Toni Gabaldon
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
pInstitució Catalana de Recerca i Estudis Avançats, 08010 Barcelona, Spain;
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James E. Tarver
qSchool of Earth Sciences, University of Bristol, BS8 1TQ, United Kingdom;
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Simon Andrews
aThe Babraham Institute, Cambridge CB22 3AT, United Kingdom;
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Heinz Himmelbauer
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
rDepartment of Biotechnology, Universität für Bodenkultur, 1190 Vienna, Austria;
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William O. H. Hughes
iInstitute of Integrative and Comparative Biology, School of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom;
sSchool of Life Sciences, University of Sussex, Brighton BN1 9QG, United Kingdom;
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Roderic Guigó
bCentre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain;
cUniversitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
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Wolf Reik
aThe Babraham Institute, Cambridge CB22 3AT, United Kingdom;
tCentre for Trophoblast Research, University of Cambridge, Cambridge CB2 3EG, United Kingdom;
uWellcome Trust Sanger Institute, Hinxton CB10 1SA, United Kingdom
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  • For correspondence: solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk
Seirian Sumner
dSchool of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
hInstitute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom;
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  • For correspondence: solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk
  1. Edited by Joan E. Strassmann, Washington University in St. Louis, St. Louis, MO, and approved September 16, 2015 (received for review August 11, 2015)

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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.

  • social evolution
  • phenotypic plasticity
  • genome sequencing
  • transcriptomes
  • DNA methylation

Footnotes

  • ↵1To whom correspondence may be addressed. Email: solenn.patalano{at}babraham.ac.uk, wolf.reik{at}babraham.ac.uk, or seirian.sumner{at}bristol.ac.uk.
  • Author contributions: S.P., C.L.A., J.E.T., S.A., W.O.H.H., R.G., W.R., and S.S. designed research; S.P., A.V., C.W., P.E., C.L.A., T.P.J., M.B., F.K., F.S.N., T.G., J.E.T., W.O.H.H., R.G., and S.S. performed research; S.P., H.H., W.O.H.H., R.G., W.R., and S.S. contributed new reagents/analytic tools; S.P., A.V., C.W., P.E., F.C., P.G.F., T.P.J., A.S.-P., M.B., I.G.-N., A.E.M., F.K., E.L., M.M.-H., J.L.R.-A., S.B., T.G., J.E.T., S.A., H.H., W.R., and S.S. analyzed data; and S.P., W.O.H.H., W.R., and S.S. wrote the paper.

  • 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.

  • This article is a PNAS Direct Submission.

  • 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).

  • See Commentary on page 13755.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1515937112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Molecular signatures of plastic phenotypes
Solenn Patalano, Anna Vlasova, Chris Wyatt, Philip Ewels, Francisco Camara, Pedro G. Ferreira, Claire L. Asher, Tomasz P. Jurkowski, Anne Segonds-Pichon, Martin Bachman, Irene González-Navarrete, André E. Minoche, Felix Krueger, Ernesto Lowy, Marina Marcet-Houben, Jose Luis Rodriguez-Ales, Fabio S. Nascimento, Shankar Balasubramanian, Toni Gabaldon, James E. Tarver, Simon Andrews, Heinz Himmelbauer, William O. H. Hughes, Roderic Guigó, Wolf Reik, Seirian Sumner
Proceedings of the National Academy of Sciences Nov 2015, 112 (45) 13970-13975; DOI: 10.1073/pnas.1515937112

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Molecular signatures of plastic phenotypes
Solenn Patalano, Anna Vlasova, Chris Wyatt, Philip Ewels, Francisco Camara, Pedro G. Ferreira, Claire L. Asher, Tomasz P. Jurkowski, Anne Segonds-Pichon, Martin Bachman, Irene González-Navarrete, André E. Minoche, Felix Krueger, Ernesto Lowy, Marina Marcet-Houben, Jose Luis Rodriguez-Ales, Fabio S. Nascimento, Shankar Balasubramanian, Toni Gabaldon, James E. Tarver, Simon Andrews, Heinz Himmelbauer, William O. H. Hughes, Roderic Guigó, Wolf Reik, Seirian Sumner
Proceedings of the National Academy of Sciences Nov 2015, 112 (45) 13970-13975; DOI: 10.1073/pnas.1515937112
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Article Classifications

  • Biological Sciences
  • Genetics

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  • Genetic architecure of eusocial insects
    - Oct 30, 2015
Proceedings of the National Academy of Sciences: 112 (45)
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  • Article
    • Abstract
    • Results and Discussion
    • Summary and Conclusions
    • Methods
    • SI Text
    • I. Sample Collections
    • II. Genome Sequencing and Annotation
    • III. Phenotype-Specific Transcriptome Sequencing and Analyses for P. canadensis and D. quadriceps
    • IV. Phenotype-Specific Methylome Sequencing and Analyses for P. canadensis and D. quadriceps
    • V. MicroRNA Sequencing and Analyses for P. canadensis and D. quadriceps
    • Acknowledgments
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