- The effect of DNA methylation on bumblebee colony development. - Chemically altered DNA methylation levels have shown clear changes in the dominance and reproductive behavior of workers in queen-less colonies, but the global effect of DNA methylation on caste determination and colony development remains unclear, mainly because of. - difficulties in controlling for genetic differences among experimental subjects in the parental line. - Here, we investigated the effect of the methylation altering agent decitabine on the developmental rate of full bumblebee colonies. - Results: Our results showed fewer methylated loci in the control group. - In insects, DNA methylation levels are often low (less than 1. - While DNA methylation at gene promoter regions suggests gene silencing as the main function, as proposed. - The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. - Full list of author information is available at the end of the article. - How- ever, in the particular case of insects such as bumblebees, differentially expressed genes contain lower levels of methylation compared to non-differentially expressed genes, which further indicates that DNA methylation in bumblebees is more related to gene expression than to an alteration of gene function [14, 15].. - One of the most defining characteristic of insect soci- eties is the reproductive division of labor, where workers usually do not produce offspring in the presence of a queen [16]. - In bumblebees, altruistic worker behavior can be explained by the higher relatedness of the female sisters, who would share ¾ of their genome, compared to the relatedness of the workers to their own male progeny. - The annual colony life cycle of a bumblebee is therefore divided into a cooperative phase, when female workers are produced while the queen has absolute reproductive dominance, and a highly aggressive compe- tition phase later in the season when the workers and queen compete over male production [19]. - Moreover, queen-less workers whose genomes had been experimentally altered by using an inhibitor of DNA methyl-transferase were more aggressive and more likely to develop ovaries compared with control queen-less workers [7], indicating that DNA methylation is important in this highly plastic re- productive division of labor. - However, these results also indicate that variation in DNA methylation levels could affect overall colony development: if workers with low DNA methylation levels gain dominance and are more keen to reproduce, the resulting colonies would show an earlier disruption of the cooperation phase, which in turn would lead to a higher production of males and a decreased production of queens [19], but see [21]. - While this ensures that all individuals have the same genotype, the absence of the queen is a rather unnatural situation that may have a profound impact on the results.. - Previous work on honeybees has shown that changes in methylation levels are involved in the switch between workers and queens [23]. - In addition, substantial differentially methylated genes were found among different castes in the termite Zootermop- sis nevadensis [25] and the ant Camponotus floridanus [26]. - DNA methylation could also be involved in worker vs. - In this study, we tested the hypothesis that DNA methylation had a significant effect on colony develop- ment of the bumblebee Bombus terrestris . - terrestris founders to the methylation disruptor decitabine through sugar water provisions, we first investigated the effect of DNA methylation on the developmental fate of larvae, and how this affected colony development. - Second, to iden- tify the specific loci that were affected by the addition of decitabine and the biological pathways these genes were involved in, brain tissue samples were collected from adult workers to be examined for DNA methylation at single base resolution using whole genome bisulfite se- quencing (WGBS).. - In agreement with the end of the cooperative phase of the colony, differences were more pronounced when colonies were counted 8 weeks after colony start-up (Z. - However, the overall effect of the treatment on male production did not reach statis- tical significance ( χ P = 0.204).. - Egg dumping behaviour was observed in 2/6 (control) and 1/5 (treated) of the colonies, which led to similar oc- currence of this behaviour among experimental groups (odds ratio = 1.879, P = 1).. - Of the significantly methylated loci, methylation fraction (number of C reads / total number of reads) appears to be similar between treated and control groups. - 10%, q = 0.05) showed significant methylation differences in the CpG context between treated and control groups. - Previous studies on honey- bees have shown that DNA methylation affects larval. - terrestris belonging to the same single parental line by using decitabine in order to infer the role of DNA methylation on phenotypic features such as caste determination and reproductive behaviour.. - Furthermore, the efficacy of the treatment was tested for a random subset of workers by analysing their methylomes using WGBS (see graphical summary in Supplementary Material).. - In absence of gen- etic differences among queen founders, and considering that there were no temporal differences for the succes- sion of main colony events, such an effect was mainly due to a higher egg-laying activity by the queen itself, combined with the higher maturation success of the queen brood. - Gene ontology for the set of differentially methylated genes in the queen female offspring included Table 1 Overview of mapping efficiency, methylation rates in CpG, CHG and CHH contexts, number of significantly methylated loci and methylation fraction per loci for the 14 workers subjected to WGBS. - Table 2 GO enrichment analysis- biological processes (BP) terms of the set of differentially methylated loci for treated and untreated workers at 10% methylation difference threshold. - In our experiment, we did not analyse direct effects of decitabine on the queen methylomes, as this would have precluded the completion of the experiment itself, and therefore we cannot assess how founder queens responded to decitabine at a molecular level. - However, workers were certainly exposed to the effect of the chemical, and therefore a more collaborative behaviour by the treated workers (less dominance, more nursing activity, etc.) might lead to the development of a bigger brood by the queen. - This finding is in contrast with the higher aggressiveness, dominance and reproductive behaviour exhibited by workers when exposed to decita- bine in absence of the founder queen (7). - In queen-right colonies, this behavior would translate into early disrup- tion of the cooperation phase and more abundant male production at the colony level [35]. - DNA Methylation is a major component of the imprint- ing systems in mammals and flowering plants [37].. - [38], who suggested that decitabine has an overall anti- metabolic activity that leads to a decline of the physical condition of the insects, and therefore results in phenotypic differences among treatments that are not dependent on DNA methylation. - Due to its antimicrobial activity, low concentrations of acetic acid are commonly used in the food industry as preserving agent, suggesting that addition of acetic acid could have af- fected the symbiotic gut flora of the queens [39, 40]. - hibernating queens represent a sensitive stage in the colony cycle in terms of survival [41] and therefore the applied treatments, or the resulting changes in gut flora, may have affected colony initiation or even caused death. - Moreover, our data have shown that the use of decitabine translates into differences in methylation patterns between the two experimental groups, including processes related to oogenesis, which also contradicts a cytotoxic role of the compound.. - Caste determination in bumble- bees has been classically assumed to be controlled by the action of queen pheromones and the endocrine profile of the larvae itself [43, 45]. - DNA methylation patterns in bumblebees. - In invertebrates, levels of DNA methylation are much lower than in vertebrates [47, 48]. - In insects, DNA methylation is concentrated in gene bodies and associ- ated with more stable patterns of gene expression [48].. - The average cytosine methylation (CpG) in the genome of honeybees is 0.7%, and much lower figures for the other methylation types (less than 0.2%) [49]. - in the control group, and similar methylation rates for the other methylation types. - Because we used founder queens from a pure genetic line, they do not differ (at least significantly) in their genetic information, making them excellent models to assess phenotypic effects of the methylation differences we experimentally induced. - The wasp Nasonia has emerged as a model for DNA methylation studies in in- sects, due to its naturally inbred nature [30]. - Despite this controversy, the lat- est evidence from honeybees suggests that even though gene body CpG methylation can oscillate during devel- opment, it is kept mostly invariable in the germline, likely to preserve function and methylation patterns over generations [49]. - Considering that the effect of the drug seems to be context-dependent [34], future studies that aim to ma- nipulate phenotypes by using decitabine should carefully check the effect of the compound at the molecular level using the best resolution available.. - Therefore, it is likely that treated bees showed higher expression levels of the differentially methylated genes.. - Our GO enrichment analyses were suggestive of a non- random effect of decitabine in the identification of DML related to oogenesis regulation and oocyte mRNA localisation. - There is increasing evidence that DNA methylation has a pronounced impact on the phenotype expressed by insects [57]. - In the particular case of social insects, epigenetically-driven phenotypic differences may be par- ticularly important, as they may affect the different roles that colony members with identical genetic information play within the colony organization. - Addition of the chemical resulted in altered DNA methylation patterns that led to a set of differentially methylated loci (with smaller methylation levels at the treated group) including some oogenesis. - Males were obtained from separate colonies of the same ori- ginal population, and they were discarded after one mat- ing event. - Neither the treatment nor the control colonies that received the sugar treatment from the first week after the start of the experiment did de- velop properly. - Just 1 out of 6 queens receiving the treat- ment managed to lay eggs and start a colony, while this number was 0 out of 6 in the control group. - Because similar effects were found for the control and treatment colonies, we conclude that the addition of the solvent to the sugar solution had a deleterious effect on the survival/fitness of queens shortly after hibernation.. - In addition, the behavior of the colony was recorded by observing colonies twice a week for 15 min throughout the trial. - Egg dumping was expressed through bees placing abandoned eggs on top of the sugar water reservoir.. - DNA methylation on workers. - DNA methylation analyses. - GO enrichment was conducted against all RNA features in the bumblebee genome using GOStats [63] to conduct a hypergeometric test, with significant GO terms identified using Benjamini-Hochberg correc- tion (adjusted p -value 0.05).. - This funding agency has no role in the design of the study, the interpretation of the data, and the preparation of the manuscript.. - Other data and scripts generated or analysed during this study are included in the submission as supplementary information files.. - DNA methylation differs between prickly and nonprickly leaves in heterophyllous Ilex aquifolium (Aquifoliaceae) trees. - Jack of all nectars, master of most: DNA methylation and the epigenetic basis of niche width in a flower-living yeast.. - Methylation and worker reproduction in the bumble-bee (Bombus terrestris). - DNA methylation: an introduction to the biology and the disease- associated changes of a promising biomarker. - Genome-wide evolutionary analysis of eukaryotic DNA methylation. - Function and evolution of DNA methylation in Nasonia vitripennis. - Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. - Evolutionary insights into DNA methylation in insects. - Dominance orders, worker reproduction, and queen-worker conflict in the slave-making ant Harpagoxenus sublaevis. - Nutritional control of reproductive status in honeybees via DNA methylation. - DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. - The caste-and sex-specific DNA methylome of the termite Zootermopsis nevadensis. - Epigenetic variation in the Egfr gene generates quantitative variation in a complex trait in ants. - Genome, transcriptome and methylome sequencing of a primitively eusocial wasp reveal a greatly reduced DNA methylation system in a social insect. - Parent-of-origin effects on genome-wide DNA methylation in the cape honey bee (Apis mellifera capensis) may be confounded by allele-specific methylation. - Allele-specific transcriptome and methylome analysis reveals stable inheritance and cis-regulation of DNA methylation in Nasonia. - DNA methylation and sex allocation in the parasitoid wasp Nasonia vitripennis. - Genome-wide disruption of DNA methylation by 5-aza-2 ’ deoxycytidine in the parasitoid wasp Nasonia vitripennis. - The evolving functions of DNA methylation. - Impact of sugar syrup and pollen diet on the bacterial diversity in the gut of indoor-reared bumblebees (Bombus terrestris). - Surviving in the absence of flowers: do nectar yeasts rely on overwintering bumblebee queens to complete their annual life cycle?. - Morphological and physiological differentiation of the caste in the bumblebee species Bombus hypnorum (L.) and Bombus terrestris (L. - Unterschiede in der Kastendetermination zwischen den Hummelarten Bombus hypnorum und Bombus terrestris/differences in the caste determination between the bumblebee species Bombus hypnorum and Bombus terrestris. - Effect of juvenile hormone on caste determination and colony processes in the bumblebee Bombus terrestris.. - DNA methylation in insects:. - on the brink of the epigenomic era. - Evolution of DNA methylation across insects. - DNA methylation is maintained with high fidelity in the honey bee germline and exhibits global non-functional fluctuations during somatic development. - Decitabine: a historical review of the development of an epigenetic drug. - DNA methylation affects the lifespan of honey bee (Apis mellifera L.) workers – evidence for a regulatory module that involves vitellogenin expression but is independent of juvenile hormone function. - 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