Bumblebee Workers Show Differences in Allele-Specific DNA Methylation and Allele-Specific Expression

Abstract

Allele-specific expression is when one allele of a gene shows higher levels of expression compared to the other allele, in a diploid organism. Recent work has identified allele-specific expression in a number of Hymenopteran species. However, the molecular mechanism which drives this allelic expression bias remains unknown. In mammals DNA methylation is often associated with genes which show allele-specific expression. DNA methylation systems have been described in species of Hymenoptera, providing a candidate mechanism. Using previously generated RNA-Seq and whole genome bisulfite sequencing from reproductive and sterile bumblebee (Bombus terrestris) workers we have identified genome-wide allele-specific expression and allele-specific DNA methylation. The majority of genes displaying allele-specific expression are common between reproductive and sterile workers and the proportion of allele-specific expression bias generally varies between genetically distinct colonies. We have also identified genome-wide allele-specific DNA methylation patterns in both reproductive and sterile workers, with reproductive workers showing significantly more genes with allele-specific methylation. Finally, there is no significant overlap between genes showing allele-specific expression and allele-specific methylation. These results indicate that cis-acting DNA methylation does not directly drive genome-wide allele-specific expression in this species.

Tissue‐specific transcription patterns support the kinship theory of intragenomic conflict in honey bees (Apis mellifera)

“…While there is evidence for parent‐specific gene methylation in honey bee workers, this variation in methylation does not correlate with parent‐specific gene expression patterns (Wu et al, 2020). Similar results were obtained in bumble bees (Marshall, Jones, et al, 2020). Other epigenetic processes, such as histone modification, can be maintained across cell divisions or removed to create tissue‐specific patterns (Galbraith, Yi, et al, 2016).…”

“…As more data are collected on intragenomic conflict using a broader array of genotypes, it will be important to determine if this pattern is consistent, and to understand the underlying mechanisms. Indeed, studies in bumble bees found substantial variation in the numbers of genes showing allelic bias in bees from different colonies (Marshall et al, 2020). It is possible that parent‐specific expression is quite widespread and includes a broader array of genes identified in this study, but these expression patterns are genotype‐specific, and thus may provide evidence for rapid evolution of these processes.…”

DNA methylation is not a driver of gene expression reprogramming in young honey bee workers

“…Therefore, these data provide strong support for the hypothesis that intragenic CpG methylation is not a driver of gene expression reprograming in the brain and ovary of young honey bees. This result is actually in line with and likely generalizable for other social insects (31,32,34,41,43,44,58).…”

“…More recent studies, however, now cast doubt on the role of gene body DNA methylation as a flexible regulator of gene expression in social insects, and an emerging consensus is that DNA methylation is genotype-specific (30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41). For example, a reanalysis of the Dnmt3 knockdown data of Li-Byarlay et al (2013) suggested that the original analysis had overestimated the number of regulated genes, and that the Dnmt3 knockdown had in fact only a minor effect on the honey bee gene body methylation pattern, and hence, on gene expression (37).…”

Intergenerational transfer of DNA methylation marks in the honey bee

“…DNA methylation states are often influenced by the underlying DNA sequence (22,23). This phenomenon is particularly prevalent in insects (21,(24)(25)(26)(27) and can be a serious confounding factor when not controlled by appropriate experimental design (28).…”