A honeybee society is organized into distinct castes, where a male embryo becomes a drone and a female embryo can develop into a queen or worker. While a queen’s role is to reproduce, the behavior of a worker varies throughout its lifetime. A worker’s first role is to act as a nurse to care for other bees in the hive, and after approximately 22 days, it becomes a forager and collects food outside the hive. Previous studies have shown that the transition from nursing to foraging requires changes in gene expression in the brain. Due to all members of the colony being offspring of the same queen, the genotypes of bees in a hive are nearly identical, suggesting that epigenetics may play a role in shaping behavioral phenotypes. A recent study published by Herb et al. showed that DNA methylation can be used to distinguish subclasses of workers and is a dynamic modification that correlates with changes in behavior.
Using whole genome bisulfite sequencing (WGBS) and comprehensive high-throughput array-based relative methylation (CHARM) analysis, the authors determined there was no difference in DNA methylation levels in the brains of newly emerged queens and workers. However, comparison of nurses to foragers revealed over 150 differentially methylated regions (DMRs) located in areas associated with transcriptional control and chromatin remodeling. To investigate further, the authors used “hive trickery” to make foragers return to a hive with only a queen and larvae, so the lack of nurses induces some foragers to revert back to nurses. As a result, over a hundred forager-to-nurse DMRs were identified. Interestingly, over half of these DMRs overlapped the initial nurse-to-forager comparison, indicating DNA methylation patterns specific to nursing bees were largely restored in reverted nurses. Further analysis showed that these epigenetically reversible genes were important for development, ATP binding, and nuclear pore formation. The authors believe these genes may influence global changes in gene expression, which contributes to the phenotype shift. Furthermore, RNA sequencing analysis showed some reverted DMRs were associated with alternative splicing events, suggesting a potential role for DNA methylation in regulating gene expression by alternative splicing.
Taken together, these results suggest distinct and complex behavioral phenotypes are associated with specific methylation patterns, which may help regulate genes important for inducing phenotype changes. This study provides the first evidence linking reversible DNA methylation to changes in behavioral phenotype. Although these findings give proof that epigenetics plays an important role in shaping an organism’s behavior, it still has to be determined which is the cause and the effect. Do you think changes in DNA methylation causes behavioral shifts or do you think behavioral shifts cause changes in DNA methylation?
Full reference: Herb et al. (2012) Reversible switching between epigenetic states in honeybee behavioral subcastes. Nature Neurosci. doi:10.1038/nn.3218 (published online September 16, 2012).
Link to abstract: http://www.nature.com/neuro/journal/v15/n10/full/nn.3218.html