Eusocial insects as emerging models for behavioural epigenetics

Yan, Hua; Simola, Daniel F.; Bonasio, Roberto; Liebig, Jürgen; Berger, Shelley L.; Reinberg, Danny

doi:10.1038/nrg3787

Cited by 185 publications

(177 citation statements)

References 156 publications

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“…Our two study species (the dinosaur ant Dinoponera quadriceps and the paper wasp Polistes canadensis) exhibit very simple societies, where individuals retain the ability to switch phenotype (11,12). This characteristic contrasts with the adult honey bee Apis mellifera and most ants, which exhibit low levels of phenotypic plasticity and have been the focus of most previous molecular analyses (13). Our two study species share similar levels of plasticity among individuals, with a single reproductive egg-layer ("gamergate" in D. quadriceps and "queen" in P. canadensis) that is morphologically identical to the nonreproductives; if the reproductive dies, it is quickly replaced by one of the nonreproductives.…”

Section: Significancementioning

confidence: 59%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

200

278

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Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

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Section: Significancementioning

confidence: 59%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

200

278

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“…However, studies in social insects have implicated the dynamics of DNA methylation in caste determination (46,47) and epigenetic changes in gene expression between tissues and sexes, as well as in differential splicing (reviewed in ref. 24). Support for a role of DNA methylation in differential gene expression of social insects includes pharmacological disruptions of DNA methylation and RNA interference knockdowns of DNA methyltransferases that alter gene expression (48).…”

Section: Resultsmentioning

confidence: 99%

“…In insects, little is known about the epigenetic differences between the two sexes and how they relate to the sex-biased expression because most sex-biased expression studies have been conducted in Drosophila, which lacks CpG methylation (22), with only low levels of methylation on adenines (6mA) in embryonic stage (23). Among social insects (bees and ants) various experiments have suggested a role for DNA methylation in regulating changes in gene expression level and splicing (24,25). In addition, a recent study suggests that differences in DNA methylation may be associated with ploidy regulation in the ant Solenopsis invicta (26).…”

mentioning

confidence: 99%

Genetic and epigenetic architecture of sex-biased expression in the jewel wasps Nasonia vitripennis and giraulti

Wang

Werren

Clark

2015

Proc. Natl. Acad. Sci. U.S.A.

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There is extraordinary diversity in sexual dimorphism (SD) among animals, but little is known about its epigenetic basis. To study the epigenetic architecture of SD in a haplodiploid system, we performed RNA-seq and whole-genome bisulfite sequencing of adult females and males from two closely related parasitoid wasps, Nasonia vitripennis and Nasonia giraulti. More than 75% of expressed genes displayed significantly sex-biased expression. As a consequence, expression profiles are more similar between species within each sex than between sexes within each species. Furthermore, extremely male-and female-biased genes are enriched for totally different functional categories: male-biased genes for key enzymes in sexpheromone synthesis and female-biased genes for genes involved in epigenetic regulation of gene expression. Remarkably, just 70 highly expressed, extremely male-biased genes account for 10% of all transcripts in adult males. Unlike expression profiles, DNA methylomes are highly similar between sexes within species, with no consistent sex differences in methylation found. Therefore, methylation changes cannot explain the extensive level of sex-biased gene expression observed. Female-biased genes have smaller sequence divergence between species, higher conservation to other hymenopterans, and a broader expression range across development. Overall, female-biased genes have been recruited from genes with more conserved and broadly expressing "house-keeping" functions, whereas male-biased genes are more recently evolved and are predominately testis specific. In summary, Nasonia accomplish a striking degree of sex-biased expression without sex chromosomes or epigenetic differences in methylation. We propose that methylation provides a general signal for constitutive gene expression, whereas other sex-specific signals cause sex-biased gene expression.sex-biased expression | DNA methylation | RNA-seq | WGBS-seq | fatty acid desaturase

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“…This task allocation also involves modification of methylation patterns in some social hymenoptera (‏Yan et al. 2014), including two species of ants (Bonasio et al. 2012) and honeybees (Herb et al.…”

Section: Introductionmentioning

confidence: 99%

Genome methylation patterns across castes and generations in a parasitoid wasp

Shaham

Ben‐Shlomo

Motro

et al. 2016

Ecology and Evolution

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Environmental influences shape phenotypes within and across generations, often through DNA methylations that modify gene expression. Methylations were proposed to mediate caste and task allocation in some eusocial insects, but how an insect's environment affects DNA methylation in its offspring is yet unknown. We characterized parental effects on methylation profiles in the polyembryonic parasitoid wasp Copidosoma koehleri, as well as methylation patterns associated with its simple caste system. We used methylation‐sensitive amplified fragment length polymorphism (MS‐AFLP) to compare methylation patterns, among (1) reproductive and soldier larvae; and (2) offspring (larvae, pupae, and adults) of wasps that were reared at either high or low larval density and mated in the four possible combinations. Methylation frequencies were similar across castes, but the profiles of methylated fragments differed significantly. Parental rearing density did not affect methylation frequencies in the offspring at any developmental stage. Principal coordinate analysis indicated no significant differences in methylation profiles among the four crossbreeding groups and the three developmental stages. Nevertheless, a clustering analysis, performed on a subset of the fragments, revealed similar methylation patterns in larvae, pupae, and adults in two of the four parental crosses. Nine fragments were methylated at two cytosine sites in all larvae, and five others were methylated at two sites in all adults. Thus, DNA methylations correlate with within‐generation phenotypic plasticity due to caste. However, their association with developmental stage and with transgenerational epigenetic effects is not clearly supported.

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Eusocial insects as emerging models for behavioural epigenetics

Cited by 185 publications

References 156 publications

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Genetic and epigenetic architecture of sex-biased expression in the jewel wasps Nasonia vitripennis and giraulti

Genome methylation patterns across castes and generations in a parasitoid wasp

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