scholarly journals Epigenetics in Social Insects: A New Direction for Understanding the Evolution of Castes

2012 ◽  
Vol 2012 ◽  
pp. 1-11 ◽  
Author(s):  
Susan A. Weiner ◽  
Amy L. Toth

Epigenetic modifications to DNA, such as DNA methylation, can expand a genome’s regulatory flexibility, and thus may contribute to the evolution of phenotypic plasticity. Recent work has demonstrated the importance of DNA methylation in alternative queen and worker “castes” in social insects, particularly honeybees. Social insects are an excellent system for addressing questions about epigenetics and evolution because: (1) they have dramatic caste polyphenisms that appear to be tied to differential methylation, (2) DNA methylation is widespread in various groups of social insects, and (3) there are intriguing connections between the social environment and DNA methylation in many species, from insects to mammals. In this article, we review research on honeybees, and, when available, other social insects, on DNA methylation and queen and worker caste differences. We outline a conceptual framework for the effects of methylation on caste determination in honeybees that may help guide studies of epigenetic regulation in other polyphenic taxa. Finally, we suggest future paths of study for social insect epigenetic research, including the importance of comparative studies of DNA methylation on a broader range of species, and highlight some key unanswered mechanistic questions about how DNA methylation affects gene regulation.

2007 ◽  
Vol 3 (5) ◽  
pp. 513-516 ◽  
Author(s):  
Rodolfo Jaffé ◽  
Daniel J.C Kronauer ◽  
F Bernhard Kraus ◽  
Jacobus J Boomsma ◽  
Robin F.A Moritz

Elaborate division of labour has contributed significantly to the ecological success of social insects. Division of labour is achieved either by behavioural task specialization or by morphological specialization of colony members. In physical caste systems, the diet and rearing environment of developing larvae is known to determine the phenotype of adult individuals, but recent studies have shown that genetic components also contribute to the determination of worker caste. One of the most extreme cases of worker caste differentiation occurs in the army ant genus Eciton , where queens mate with many males and colonies are therefore composed of numerous full-sister subfamilies. This high intracolonial genetic diversity, in combination with the extreme caste polymorphism, provides an excellent test system for studying the extent to which caste determination is genetically controlled. Here we show that genetic effects contribute significantly to worker caste fate in Eciton burchellii . We conclude that the combination of polyandry and genetic variation for caste determination may have facilitated the evolution of worker caste diversity in some lineages of social insects.


2019 ◽  
Author(s):  
Hollie Marshall ◽  
Zoë N. Lonsdale ◽  
Eamonn B. Mallon

AbstractPhenotypic plasticity is the production of multiple phenotypes from a single genome and is notably observed in social insects. Multiple epigenetic mechanisms have been associated with social insect plasticity, with DNA methylation being explored to the greatest extent. DNA methylation is thought to play a role in caste determination in Apis mellifera, and other social insects, but there is limited knowledge on it’s role in other bee species. In this study we analysed whole genome bisulfite sequencing and RNA-seq data sets from head tissue of reproductive and sterile castes of the eusocial bumblebee Bombus terrestris. We found genome-wide methylation in B. terrestris is similar to other social insects and does not differ between reproductive castes. We did, however, find differentially methylated genes between castes, which are enriched for multiple biological processes including reproduction. However we found no relationship between differential methylation and differential gene expression or differential exon usage between castes. Our results also indicate high inter-colony variation in methylation. These findings suggest methylation is associated with caste differences but may serve an alternate function, other than direct caste determination in this species. This study provides the first insights into the nature of a bumblebee caste specific methylome as well as it’s interaction with gene expression and caste specific alternative splicing, providing greater understanding of the role of methylation in phenotypic plasticity within social bee species. Future experimental work is needed to determine the function of methylation and other epigenetic mechanisms in social insects.Impact SummarySocial insects, such as ants, termites, bees and wasps, can produce individuals with extreme physical and behavioural differences within the same colony known as castes (e.g. workers/soldiers/queens). These individuals have similar genomes and many studies have associated epigenetic mechanisms with the differences observed. Epigenetic modifications are changes that affect how genes are expressed without changing the underlying DNA code. Here we investigated differences in DNA methylation (a well researched modified base) between different reproductive castes of the bumblebee, Bombus terrestris, an economically and environmentally important pollinator species. We found B. terrestris has a similar methylation profile to other social insect species in terms of the distribution of methylation throughout the genome and the relationship between methylation and gene expression. Genes that have differences in methylation between reproductive castes are involved in multiple biological processes, including reproduction, suggesting methylation may hold multiple functions in this species. These differentially methylated genes are also different to differentially methylated genes identified between honeybee reproductive castes, again suggesting methylation may have a variable function. These findings provide greater understanding of the role of methylation in caste determination in social insect species.


2007 ◽  
Vol 274 (1618) ◽  
pp. 1625-1630 ◽  
Author(s):  
William O.H Hughes ◽  
Jacobus J Boomsma

Advanced societies owe their success to an efficient division of labour that, in some social insects, is based on specialized worker phenotypes. The system of caste determination in such species is therefore critical. Here, we examine in a leaf-cutting ant ( Acromyrmex echinatior ) how a recently discovered genetic influence on caste determination interacts with the social environment. By removing most of one phenotype (large workers; LW) from test colonies, we increased the stimulus for larvae to develop into this caste, while for control colonies we removed a representative sample of all workers so that the stimulus was unchanged. We established the relative tendencies of genotypes to develop into LW by genotyping workers before and after the manipulation. In the control colonies, genotypes were similarly represented in the large worker caste before and after worker removal. In the test colonies, however, this relationship was significantly weaker, demonstrating that the change in environmental stimuli had altered the caste propensity of at least some genotypes. The results indicate that the genetic influence on worker caste determination acts via genotypes differing in their response thresholds to environmental cues and can be conceptualized as a set of overlapping reaction norms. A plastic genetic influence on division of labour has thus evolved convergently in two distantly related polyandrous taxa, the leaf-cutting ants and the honeybees, suggesting that it may be a common, potentially adaptive, property of complex, genetically diverse societies.


2010 ◽  
Vol 6 (6) ◽  
pp. 800-802 ◽  
Author(s):  
Jennie J. Kuzdzal-Fick ◽  
David C. Queller ◽  
Joan E. Strassmann

Greater size and strength are common attributes of contest winners. Even in social insects with high cooperation, the right to reproduce falls to the well-fed queens rather than to poorly fed workers. In Dictyostelium discoideum , formerly solitary amoebae aggregate when faced with starvation, and some cells die to form a stalk which others ride up to reach a better location to sporulate. The first cells to starve have lower energy reserves than those that starve later, and previous studies have shown that the better-fed cells in a mix tend to form disproportionately more reproductive spores. Therefore, one might expect that the first cells to starve and initiate the social stage should act altruistically and form disproportionately more of the sterile stalk, thereby enticing other better-fed cells into joining the aggregate. This would resemble caste determination in social insects, where altruistic workers are typically fed less than reproductive queens. However, we show that the opposite result holds: the first cells to starve become reproductive spores, presumably by gearing up for competition and outcompeting late starvers to become prespore first. These findings pose the interesting question of why others would join selfish organizers.


2021 ◽  
Vol 22 (6) ◽  
pp. 2790
Author(s):  
Steffan Noe Christiansen ◽  
Stine Bøttcher Jacobsen ◽  
Jeppe Dyrberg Andersen ◽  
Marie-Louise Kampmann ◽  
Linea Christine Trudsø ◽  
...  

Sudden cardiac death (SCD) is a diagnostic challenge in forensic medicine. In a relatively large proportion of the SCDs, the deaths remain unexplained after autopsy. This challenge is likely caused by unknown disease mechanisms. Changes in DNA methylation have been associated with several heart diseases, but the role of DNA methylation in SCD is unknown. In this study, we investigated DNA methylation in two SCD subtypes, sudden unexplained death (SUD) and sudden unexpected death in epilepsy (SUDEP). We assessed DNA methylation of more than 850,000 positions in cardiac tissue from nine SUD and 14 SUDEP cases using the Illumina Infinium MethylationEPIC BeadChip. In total, six differently methylated regions (DMRs) between the SUD and SUDEP cases were identified. The DMRs were located in proximity to or overlapping genes encoding proteins that are a part of the glutathione S-transferase (GST) superfamily. Whole genome sequencing (WGS) showed that the DNA methylation alterations were not caused by genetic changes, while whole transcriptome sequencing (WTS) showed that DNA methylation was associated with expression levels of the GSTT1 gene. In conclusion, our results indicate that cardiac DNA methylation is similar in SUD and SUDEP, but with regional differential methylation in proximity to GST genes.


2021 ◽  
Vol 14 (1) ◽  
Author(s):  
Benjamin I. Laufer ◽  
J. Antonio Gomez ◽  
Julia M. Jianu ◽  
Janine M. LaSalle

Abstract Background Down syndrome (DS) is characterized by a genome-wide profile of differential DNA methylation that is skewed towards hypermethylation in most tissues, including brain, and includes pan-tissue differential methylation. The molecular mechanisms involve the overexpression of genes related to DNA methylation on chromosome 21. Here, we stably overexpressed the chromosome 21 gene DNA methyltransferase 3L (DNMT3L) in the human SH-SY5Y neuroblastoma cell line and assayed DNA methylation at over 26 million CpGs by whole genome bisulfite sequencing (WGBS) at three different developmental phases (undifferentiated, differentiating, and differentiated). Results DNMT3L overexpression resulted in global CpG and CpG island hypermethylation as well as thousands of differentially methylated regions (DMRs). The DNMT3L DMRs were skewed towards hypermethylation and mapped to genes involved in neurodevelopment, cellular signaling, and gene regulation. Consensus DNMT3L DMRs showed that cell lines clustered by genotype and then differentiation phase, demonstrating sets of common genes affected across neuronal differentiation. The hypermethylated DNMT3L DMRs from all pairwise comparisons were enriched for regions of bivalent chromatin marked by H3K4me3 as well as differentially methylated sites from previous DS studies of diverse tissues. In contrast, the hypomethylated DNMT3L DMRs from all pairwise comparisons displayed a tissue-specific profile enriched for regions of heterochromatin marked by H3K9me3 during embryonic development. Conclusions Taken together, these results support a mechanism whereby regions of bivalent chromatin that lose H3K4me3 during neuronal differentiation are targeted by excess DNMT3L and become hypermethylated. Overall, these findings demonstrate that DNMT3L overexpression during neurodevelopment recreates a facet of the genome-wide DS DNA methylation signature by targeting known genes and gene clusters that display pan-tissue differential methylation in DS.


Author(s):  
Unni Pulliainen ◽  
Nick Bos ◽  
Patrizia d’Ettorre ◽  
Liselotte Sundström

AbstractChemical communication is common across all organisms. Insects in particular use predominantly chemical stimuli in assessing their environment and recognizing their social counterparts. One of the chemical stimuli used for recognition in social insects, such as ants, is the suite of long-chain, cuticular hydrocarbons. In addition to providing waterproofing, these surface hydrocarbons serve as a signature mixture, which ants can perceive, and use to distinguish between strangers and colony mates, and to determine caste, sex, and reproductive status of another individual. They can be both environmentally and endogenously acquired. The surface chemistry of adult workers has been studied extensively in ants, yet the pupal stage has rarely been considered. Here we characterized the surface chemistry of pupae of Formica exsecta, and examine differences among sexes, castes (reproductive vs. worker), and types of sample (developing individual vs. cocoon envelope). We found quantitative and qualitative differences among both castes and types of sample, but male and female reproductives did not differ in their surface chemistry. We also found that the pupal surface chemistry was more complex than that of adult workers in this species. These results improve our understanding of the information on which ants base recognition, and highlights the diversity of surface chemistry in social insects across developmental stages.


Author(s):  
Sophia Bam ◽  
Erin Buchanan ◽  
Caitlyn Mahony ◽  
Colleen O’Ryan

Autism spectrum disorder (ASD) is a complex disorder that is underpinned by numerous dysregulated biological pathways, including pathways that affect mitochondrial function. Epigenetic mechanisms contribute to this dysregulation and DNA methylation is an important factor in the etiology of ASD. We measured DNA methylation of peroxisome proliferator-activated receptor-gamma coactivator-1 alpha (PGC-1α), as well as five genes involved in regulating mitochondrial homeostasis to examine mitochondrial dysfunction in an ASD cohort of South African children. Using targeted Next Generation bisulfite sequencing, we found differential methylation (p < 0.05) at six key genes converging on mitochondrial biogenesis, fission and fusion in ASD, namely PGC-1α, STOML2, MFN2, FIS1, OPA1, and GABPA. PGC-1α, the transcriptional regulator of biogenesis, was significantly hypermethylated at eight CpG sites in the gene promoter, one of which contained a putative binding site for CAMP response binding element 1 (CREB1) (p = 1 × 10–6). Mitochondrial DNA (mtDNA) copy number, a marker of mitochondrial function, was elevated (p = 0.002) in ASD compared to controls and correlated significantly with DNA methylation at the PGC-1α promoter and there was a positive correlation between methylation at PGC-1α CpG#1 and mtDNA copy number (Spearman’s r = 0.2, n = 49, p = 0.04) in ASD. Furthermore, DNA methylation at PGC-1α CpG#1 and mtDNA copy number correlated significantly (p < 0.05) with levels of urinary organic acids associated with mitochondrial dysfunction, oxidative stress, and neuroendocrinology. Our data show differential methylation in ASD at six key genes converging on PGC-1α-dependent regulation of mitochondrial biogenesis and function. We demonstrate that methylation at the PGC-1α promoter is associated with elevated mtDNA copy number and metabolomic evidence of mitochondrial dysfunction in ASD. This highlights an unexplored role for DNA methylation in regulating specific pathways involved in mitochondrial biogenesis, fission and fusion contributing to mitochondrial dysfunction in ASD.


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