Like father like daughter? Investigating epigenetic inheritance in honeybees

Besides their value for plant pollination, honeybees are an important model organism for studying how cooperation and conflicts are balanced in social systems. Honeybee queens mate with multiple males (drones), so each colony is comprised of up to 30 worker ‘patrilines’, each sired by a different father. Patriline-specific traits in worker physiology and behaviour are well documented, and are often interpreted as evidence of genetic task specialisation – the adaptive phenomenon in which workers with particular fathers perform specific tasks like guarding or pollen foraging. Yet the genetics of such traits are complex and the underlying causal genes are largely unknown. An underexplored avenue by which each drone could influence his worker progeny involves epigenetic mechanisms, DNA methylation being the best candidate.

DNA methylation is an epigenetic modification that alters gene expression by adding methyl marks to cytosines. DNA methylation is involved in developmental and phenotypic plasticity, and could be responsible for parent-of-origin effects. Previous results showed that male honeybees produce semen with unique DNA methylation profiles, indicating that they have the potential to epigenetically influence their worker daughters, ultimately leading to patriline-specific traits. Honeybees thus give us the unique opportunity to investigate the existence of epigenetic inheritance and its impacts on societies.

In this study we set out to investigate whether DNA methylation profiles are being transferred between generations in honey bees. After controlling for genetic and environmental effects, we found that the similarity of methylomes was much greater within patrilines than between patrilines, that is between fathers and daughters as opposed to between unrelated males and workers from the same colony. There were no major differences in the density of DNA methylation between tissues and generations. Samples from the same patriline, particularly semen and worker samples, consistently clustered together with respect to their methylation patterns. These samples shared twice as many methylated sites and had four times less differentially methylated regions compared to samples from different patrilines. Our results thus indicate that there is no epigenetic reprogramming during embryogenesis in the honey bee, and clearly show that there is an intergenerational transfer of epigenetic marks between fathers and daughters in this invertebrate.