The dynamic DNA methylation cycle from egg to sperm in the honey beeApis mellifera

Abstract

In honey bees (Apis mellifera), the epigenetic mark of DNA methylation is central to the developmental regulation of caste differentiation, but may also be involved in additional biological functions. In this study, we examine the whole genome methylation profiles of three stages of the haploid honey bee genome: unfertilised eggs, the adult drones that develop from these eggs and the sperm produced by these drones. These methylomes reveal distinct patterns of methylation. Eggs and sperm show 381 genes with significantly different CpG methylation patterns, with the vast majority being more methylated in eggs. Adult drones show greatly reduced levels of methylation across the genome when compared with both gamete samples. This suggests a dynamic cycle of methylation loss and gain through the development of the drone and during spermatogenesis. Although fluxes in methylation during embryogenesis may account for some of the differentially methylated sites, the distinct methylation patterns at some genes suggest parentspecific epigenetic marking in the gametes. Extensive germ line methylation of some genes possibly explains the lower-than-expected frequency of CpG sites in these genes. We discuss the potential developmental and evolutionary implications of methylation in eggs and sperm in this eusocial insect species.

Robust DNA Methylation in the Clonal Raider Ant Brain

“…Finally, many cytosines were methylated in one sample only, due to either biological or experimental variation. By applying the statistical methods used in previous studies [1–4, 6] to our data, we show that such sample-specific DNA methylation may underlie the previous findings of queen- and worker-specific methylation. We argue that there is currently no evidence that genome-wide variation in DNA methylation is associated with the queen and worker castes in social insects, and we call for a more careful interpretation of the available data.…”

“…There was no exon that was consistently differentially methylated between phases in all four source colonies. This shows that the statistical method used in previous studies, especially when used without biological replicates [1–4, 6], is prone to return random or colony-specific lists of exons. See also Figure S3.…”

Developmental DNA methyltransferase expression in the fire ant Solenopsis invicta

“…Although we have no direct evidence to suggest a role for DNMT1 in imprinting, it is notable that eusocial life and haplodiploidy present a number of evolutionary conflicts between males and queens (Drewell et al, 2012;Galbraith et al, 2016). Moreover, eggs and sperm have been shown to exhibit differences in DNA methylation at several hundred genes in A. mellifera (Drewell et al, 2014), and differences in the expression of A. mellifera matrigenes and patrigenes have recently been documented (Galbraith et al, 2016). Nevertheless, a recent investigation of Nasonia revealed no direct evidence for parent-of-origin differentially methylated regions, which casts doubt on the DNA methylation-imprinting hypothesis in hymenopteran insects (Wang et al, 2016).…”

“…Indeed, a previous analysis revealed rank correlations greater than 0.9 between mean coding sequence DNA methylation levels of distinct fire ant castes and sexes, as well as between A. mellifera brains and whole body samples (Table S4 in Hunt et al, 2013b). Similarly, the commonalities in DNA methylomes from A. mellifera sperm, eggs, and adult males vastly outnumber the differences (Drewell et al, 2014). Thus, we hypothesize that most de novo DNA methylation occurs during embryonic, rather than postembryonic, development, and that DNMT3 is performing de novo DNA methylation in S. invicta.…”

Inheritance of thelytoky in the honey bee Apis mellifera capensis

“…Similarly, aspects of honey bee defensiveness (Guzman-Novoa et al, 2005) and reproductive physiology (Jordan et al, 2008a;Linksvayer et al, 2009;Beekman et al, 2012;Oldroyd et al, 2014) are more strongly transmitted via males than via females. Honey bees have a fully functional DNA methylation system (Wang et al, 2006;Foret et al, 2009) and differential methylation depending on parent-of-origin could explain the observed effects of sire (Drewell et al, 2012;Drewell et al, 2014;Oldroyd et al, 2014). We found that two colonies headed by F 1 queens backcrossed to Scutellata drones produced a similar proportion of offspring thelytokously (21 thelytokous vs 6 arrhenotokous) as two colonies headed by F 1 queens backcrossed to Capensis drones (37 thelytokous vs 21 arrhenotokous; χ 2 1 = 1.662, P = 0.197).…”