Abstract
BackgroundDNA methylation is a common regulator of gene expression, including acting as a regulator of developmental events and behavioral changes in adults. Using the unique system of genetic caste determination in Pogonomyrmex barbatus, we were able to document changes in DNA methylation during development, and also across both ancient and contemporary hybridization events.Methodology/Principal FindingsSodium bisulfite sequencing demonstrated in vivo methylation of symmetric CG dinucleotides in P. barbatus. We also found methylation of non-CpG sequences. This validated two bioinformatics methods for predicting gene methylation, the bias in observed to expected ratio of CpG dinucleotides and the density of CpG/TpG single nucleotide polymorphisms (SNP). Frequencies of genomic DNA methylation were determined for different developmental stages and castes using ms-AFLP assays. The genetic caste determination system (GCD) is probably the product of an ancestral hybridization event between P. barbatus and P. rugosus. Two lineages obligately co-occur within a GCD population, and queens are derived from intra-lineage matings whereas workers are produced from inter-lineage matings. Relative DNA methylation levels of queens and workers from GCD lineages (contemporary hybrids) were not significantly different until adulthood. Virgin queens had significantly higher relative levels of DNA methylation compared to workers. Worker DNA methylation did not vary among developmental stages within each lineage, but was significantly different between the currently hybridizing lineages. Finally, workers of the two genetic caste determination lineages had half as many methylated cytosines as workers from the putative parental species, which have environmental caste determination.Conclusions/SignificanceThese results suggest that DNA methylation may be a conserved regulatory mechanism moderating division of labor in both bees and ants. Current and historic hybridization appear to have altered genomic methylation levels suggesting a possible link between changes in overall DNA methylation and the origin and regulation of genetic caste determination in P. barbatus.
Highlights
DNA methylation is a common form of epigenetic modification present in most kingdoms of life
Gene Specific in vivo Methylation We have demonstrated the validity of using CpG[o/e] values and single nucleotide polymorphisms (SNP) to predict the presence of methylated cytosines in a specific region of DNA in P. barbatus
We demonstrate using, multiple methods, that DNA methylation occurs in the red harvester ant, P. barbatus
Summary
DNA methylation is a common form of epigenetic modification present in most kingdoms of life. DNA methylation can act as a major regulator of gene expression, in some contexts regulating multiple canalized phenotypes and giving rise to developmental and behavioral variation [1,2,3,4,5,6]. The queen phenotype in honeybees can be produced via RNA interference knockdown of the enzyme responsible for de novo DNA methylation, DNMT3 [18]. This suggests that decreased de novo methylation during larval development will initiate queen development. DNA methylation is a common regulator of gene expression, including acting as a regulator of developmental events and behavioral changes in adults. Using the unique system of genetic caste determination in Pogonomyrmex barbatus, we were able to document changes in DNA methylation during development, and across both ancient and contemporary hybridization events
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