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

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Patalano, Solenn 
Vlasova, Anna 
Wyatt, Chris 
Ewels, Philip 
Camara, Francisco 

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.

DNA methylation, genome sequencing, phenotypic plasticity, social evolution, transcriptomes, Animals, Ants, Base Sequence, Brain, DNA Methylation, Gene Expression Regulation, Genome, Insect, Hierarchy, Social, High-Throughput Nucleotide Sequencing, MicroRNAs, Models, Genetic, Molecular Sequence Data, Phenotype, Social Behavior, Transcriptome, Wasps
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Proc Natl Acad Sci U S A
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Proceedings of the National Academy of Sciences
Wellcome Trust (099232/Z/12/Z)
This work was funded by NERC: NE/G000638/1, NBAF581, NE/K011316/1 (SS) and NE/G012121/1 (WOHH, SS), RCUK (SS) (SB), Leverhulme Trust (WOHH), BMBF FKZ 0315962 B & CRG core funding (HH), Spanish ministry of Economy and Competitiveness BIO2012-37161 (TG), Spanish MINECO BIO2011-26205 (RG), ISCIII PT13/0001/0021 (RG), Instituto Nacional de Bioinformatica and AGAUR (RG), Wellcome Trust 095645/Z/11/Z (WR), BBSRC BB/K010867/1 (WR), Stuttgart Universität (TPJ), Fapesp 2010/10027-5 (FSN). This work was conducted under collecting and export permits SE/A-20-12, 10BR004553/DF and 11BR006471/DF. SB is a founder and shareholder of Cambridge Epigenetix Limited. WR is a consultant and shareholder of Cambridge Epigenetix Limited. Genomic analyses were performed on the whole genome assemblies of P. canadensis and D. quadriceps, deposited at DDBJ/ EMBL/ GenBank under the accession SAMN02869711 and SAMN02869781, respectively. Raw data from all BS-seq and RNA-seq libraries were deposited in GEO under the accession number GSE59525.