Edited by Joan E. Strassmann, Washington University in St. Louis, St. Louis, MO, and approved September 16, 2015 (received for review August 11, 2015)
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.
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.
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.
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