Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies.
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.
The Babraham Institute, Cambridge CB22 3AT, United Kingdom; solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk.
Solenn
S
Patalano
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
Anna
A
Vlasova
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain; School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
Chris
C
Wyatt
The Babraham Institute, Cambridge CB22 3AT, United Kingdom; Department of Biochemistry and Biophysics, Science for Life Laboratory, Stockholm University, Stockholm 106 91, Sweden;
Philip
P
Ewels
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
Francisco
F
Camara
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Instituto de Investigação e Inovação em Saúde, Universidade do Porto, 4200-135 Porto, Portugal; Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), Institute of Molecular Pathology and Immunology, University of Porto, 4200-135 Porto, Portugal;
Pedro G
PG
Ferreira
Institute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom; Institute of Integrative and Comparative Biology, School of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom;
Claire L
CL
Asher
Institute of Biochemistry, University of Stuttgart, 70569 Stuttgart, Germany;
Tomasz P
TP
Jurkowski
The Babraham Institute, Cambridge CB22 3AT, United Kingdom;
Anne
A
Segonds-Pichon
Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom; Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge CB2 ORE, United Kingdom;
Martin
http://orcid.org/0000-0003-3903-6492
M
Bachman
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
Irene
I
González-Navarrete
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain; Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany;
André E
AE
Minoche
The Babraham Institute, Cambridge CB22 3AT, United Kingdom;
Felix
F
Krueger
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
Ernesto
E
Lowy
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
Marina
M
Marcet-Houben
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
Jose Luis
JL
Rodriguez-Ales
Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP)-Universidade de São Paulo, 14040-901, Ribeirão Preto-SP, Brazil;
Fabio S
FS
Nascimento
Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom; Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge CB2 ORE, United Kingdom; School of Clinical Medicine, University of Cambridge, CB2 0SP, Cambridge, United Kingdom;
Shankar
S
Balasubramanian
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats, 08010 Barcelona, Spain;
Toni
T
Gabaldon
School of Earth Sciences, University of Bristol, BS8 1TQ, United Kingdom;
James E
JE
Tarver
The Babraham Institute, Cambridge CB22 3AT, United Kingdom;
Simon
S
Andrews
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain; Department of Biotechnology, Universität für Bodenkultur, 1190 Vienna, Austria;
Heinz
H
Himmelbauer
Institute of Integrative and Comparative Biology, School of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom; School of Life Sciences, University of Sussex, Brighton BN1 9QG, United Kingdom;
William O H
WO
Hughes
Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
Roderic
R
Guigó
The Babraham Institute, Cambridge CB22 3AT, United Kingdom; Centre for Trophoblast Research, University of Cambridge, Cambridge CB2 3EG, United Kingdom; Wellcome Trust Sanger Institute, Hinxton CB10 1SA, United Kingdom solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk.
Wolf
W
Reik
School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom; Institute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom; solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk.
Seirian
S
Sumner
D000818:Animals; D001000:Ants / Q000235:genetics* / Q000502:physiology; D001483:Base Sequence; D001921:Brain / Q000378:metabolism; D019175:DNA Methylation / Q000235:genetics; D005786:Gene Expression Regulation / Q000235:genetics*; D049750:Genome, Insect / Q000235:genetics; D006608:Hierarchy, Social; D059014:High-Throughput Nucleotide Sequencing; D035683:MicroRNAs / Q000235:genetics; D008957:Models, Genetic; D008969:Molecular Sequence Data; D010641:Phenotype; D012919:Social Behavior; D059467:Transcriptome / Q000235:genetics; D014863:Wasps / Q000235:genetics* / Q000502:physiology
D035683:MicroRNAs
DNA methylation; genome sequencing; phenotypic plasticity; social evolution; transcriptomes