Variation in DNA methylation is not consistently reflected by sociality in hymenoptera

Karl M. Glastad, Samuel V. Arsenault, Kim L. Vertacnik, Scott M. Geib, Sasha Kay, Bryan N. Danforth, Sandra M. Rehan, Catherine R. Linnen, Sarah D. Kocher, Brendan G. Hunt

Research output: Contribution to journalArticlepeer-review

28 Scopus citations

Abstract

Changes in gene regulation that underlie phenotypic evolution can be encoded directly in the DNA sequence or mediated by chromatin modifications such as DNA methylation. It has been hypothesized that the evolution of eusocial division of labor is associated with enhanced gene regulatory potential, which may include expansions in DNA methylation in the genomes of Hymenoptera (bees, ants, wasps, and sawflies). Recently, this hypothesis garnered support from analyses of a commonly used metric to estimate DNA methylation in silico, CpG content. Here, we test this hypothesis using direct, nucleotide-level measures of DNA methylation across nine species of Hymenoptera. In doing so, we generated new DNA methylomes for three species of interest, including one solitary and one facultatively eusocial halictid bee and a sawfly. We demonstrate that the strength of correlation between CpG content and DNA methylation varies widely among hymenopteran taxa, highlighting shortcomings in the utility of CpG content as a proxy for DNA methylation in comparative studies of taxa with sparse DNA methylomes. We observed strikingly high levels of DNA methylation in the sawfly relative to other investigated hymenopterans. Analyses of molecular evolution suggest the relatively distinct sawfly DNA methylome may be associated with positive selection on functional DNMT3 domains. Sawflies are an outgroup to all ants, bees, and wasps, and no sawfly species are eusocial. We find no evidence that either global expansions or variation within individual ortholog groups in DNA methylation are consistently associated with the evolution of social behavior.

Original languageEnglish
Pages (from-to)1687-1698
Number of pages12
JournalGenome Biology and Evolution
Volume9
Issue number6
DOIs
StatePublished - Jun 1 2017

Bibliographical note

Funding Information:
This work was supported by the University of Georgia College of Agricultural and Environmental Sciences and Princeton University. We thank Mary Centrella, Achik Dorchin, and Graham Montgomery for Dufourea novaeangliae collection, John Terbot for Neodiprion lecontei collection, Adam Bewick for assistance with molecular evolution analysis, and the Georgia Advanced Computing Resource Center for computational resources and support.

Publisher Copyright:
ß The Author 2017.

Keywords

  • CpG o/e
  • Epigenetics
  • Eusociality
  • Neodiprion lecontei
  • Social insects
  • Whole genome bisulfite sequencing

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

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