Comparative Analyses of DNA Methylation and Sequence Evolution Using Nasonia Genomes

Park, Jungsun; Peng, Zuogang; Zeng, Jia; Elango, Navin; Park, Taesung; Wheeler, David A.; Werren, John H.; Yi, Soojin V.

doi:10.1093/molbev/msr168

Cited by 100 publications

(114 citation statements)

References 39 publications

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“…4a). This is revealed by CpG depletion patterns (CpG o/e , observed versus expected number of CpGs), a reliable predictor of DNA methylation 38,39 , correlating more strongly between the termites than among any of the other analysed hemimetabolous insects (Fig. 4).…”

Section: Changes In Gene Regulation In Termitesmentioning

confidence: 95%

Hemimetabolous genomes reveal molecular basis of termite eusociality

et al. 2018

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E usociality, the reproductive division of labour with overlapping generations and cooperative brood care, is one of the major evolutionary transitions in biology 1 . Although rare, eusociality has been observed in a diverse range of organisms, including shrimps, mole rats and several insect lineages [2][3][4] . A particularly striking case of convergent evolution occurred within the holometabolous Hymenoptera and in the hemimetabolous termites (Isoptera), which are separated by over 350 Myr of evolution 5 . Termites evolved within the cockroaches around 150 Myr ago, towards the end of the Jurassic period 6,7 , about 50 Myr before the first bees and ants appeared 5 . Therefore, identifying the molecular mechanisms common to both origins of eusociality is crucial to understanding the fundamental signatures of these rare evolutionary transitions. While the availability of genomes from many eusocial and non-eusocial hymenopteran species 8 has allowed extensive research into the origins of eusociality within ants and bees [9][10][11] , a paucity of genomic data from cockroaches and termites has precluded large-scale investigations into the evolution of eusociality in this hemimetabolous clade.The conditions under which eusociality arose differ greatly between the two groups. Termites and cockroaches are hemimetabolous and so show a direct development, while holometabolous hymenopterans complete the adult body plan during metamorphosis. In termites, workers are immatures and only reproductive castes are adults 12 , while in Hymenoptera, adult workers and queens represent the primary division of labour. Moreover, termites are diploid and their colonies consist of both male and female workers, and usually a queen and king dominate reproduction. This is in contrast to the haplodiploid system found in Hymenoptera, in which all workers and dominant reproductives are female. It is therefore intriguing that strong similarities have evolved convergently within the termites and the hymenopterans, such as differentiated castes and a nest life with reproductive division of labour. The termites can be subdivided into wood-dwelling and foraging termites. The former belong to the lower termites and produce simple, small colonies with totipotent workers that can become reproductives. Foraging termites (some lower and all higher termites) form large, complex societies, in which worker castes can be irreversible 12 . For this reason, higher, but not lower, termites can be classed as superorganismal 13 . Similarly, within Hymenoptera, varying levels of eusociality exist.Here we provide insights into the molecular signatures of eusociality within the termites. We analysed the genomes of two lower and one higher termite species and compared them to the genome

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Section: Changes In Gene Regulation In Termitesmentioning

confidence: 95%

Hemimetabolous genomes reveal molecular basis of termite eusociality

et al. 2018

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“…Of note, a low CpG O/E indicates a high level of C-to-T mutations, which has been reported to result mostly from DNA methylation (18,26,27). Therefore, a negative correlation between DNA methylation level and CpG O/E is expected (10,26,27). We assume that the coefficient of correlation between the two measurements reflects the proportion of methylated CpGs having actually undergone mutation.…”

Section: Mutagenic Effect Of Dna Methylation Varies Among Coding Exonsmentioning

confidence: 95%

“…S1C). In addition, both G + C content and exon length have been shown to be positively correlated with evolutionary rates (27,29). Furthermore, the factor of CSE/ASE exon type should also be controlled because mCG density is associated with the CSE/ASE exon type ( Fig.…”

Section: Mutagenic Effect Of Dna Methylation Varies Among Coding Exonsmentioning

confidence: 99%

Position-dependent correlations between DNA methylation and the evolutionary rates of mammalian coding exons

Chuang

Chen

2012

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

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DNA cytosine methylation is a central epigenetic marker that is usually mutagenic and may increase the level of sequence divergence. However, methylated genes have been reported to evolve more slowly than unmethylated genes. Hence, there is a controversy on whether DNA methylation is correlated with increased or decreased protein evolutionary rates. We hypothesize that this controversy has resulted from the differential correlations between DNA methylation and the evolutionary rates of coding exons in different genic positions. To test this hypothesis, we compare human-mouse and human-macaque exonic evolutionary rates against experimentally determined single-base resolution DNA methylation data derived from multiple human cell types. We show that DNA methylation is significantly related to within-gene variations in evolutionary rates. First, DNA methylation level is more strongly correlated with C-to-T mutations at CpG dinucleotides in the first coding exons than in the internal and last exons, although it is positively correlated with the synonymous substitution rate in all exon positions. Second, for the first exons, DNA methylation level is negatively correlated with exonic expression level, but positively correlated with both nonsynonymous substitution rate and the sample specificity of DNA methylation level. For the internal and last exons, however, we observe the opposite correlations. Our results imply that DNA methylation level is differentially correlated with the biological (and evolutionary) features of coding exons in different genic positions. The first exons appear more prone to the mutagenic effects, whereas the other exons are more influenced by the regulatory effects of DNA methylation.methylation-associated mutation | exon evolution | genomics | deep sequencing | bioinformatics D NA methylation is a common form of epigenetic modification that is important for a variety of biological functions, including transcriptional silencing (1), genomic imprinting (2), X-chromosome inactivation (3), the silencing of transposons (4), tumorigenesis (5), and the differentiation of pluripotent cells (6). DNA methylation is unevenly distributed in the human genome. For example, the CpG islands near the promoter regions of active genes tend to be unmethylated (7-10), because methylation in these regions is strongly correlated with transcriptional suppression (8). It has also been reported that exons tend to be more methylated than introns, and that sharp transitions of methylation occur at exonintron boundaries in human (6). Moreover, the level of DNA methylation also varies among exonic regions. The levels of DNA methylation in the first exons were reported to be lower than in downstream exons, and tightly linked to transcriptional silencing (11). In addition, the level of DNA methylation exhibits a slight but sharp step-down at the transcriptional terminal sites (6).In terms of molecular evolution, DNA methylation is relevant in two aspects. First, DNA methylation can significantly increase the rate of spontan...

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“…2015), and in a number of wasp species (Park et al. 2011). DNA methylation is potentially important in shaping phenotypes and adaptations to the environment, such as in caste determination in eusocial species (Smith et al.…”

Section: Introductionmentioning

confidence: 99%

“…DNA methylation is prevalent in the N. vitripennis genome, mainly in exons, and is correlated with elevated gene expression and with genes that are expressed in all developmental stages (Park et al. 2011; Wang et al. 2013).…”

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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Comparative Analyses of DNA Methylation and Sequence Evolution Using Nasonia Genomes

Cited by 100 publications

References 39 publications

Hemimetabolous genomes reveal molecular basis of termite eusociality

Hemimetabolous genomes reveal molecular basis of termite eusociality

Position-dependent correlations between DNA methylation and the evolutionary rates of mammalian coding exons

Genome methylation patterns across castes and generations in a parasitoid wasp

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