The role of plastic and evolved<scp>DNA</scp>methylation in parallel adaptation of threespine stickleback (<i>Gasterosteus aculeatus</i>)

Hu, Juntao; Barrett, Rowan D. H.

doi:10.1111/mec.16832

Cited by 9 publications

(6 citation statements)

References 110 publications

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“…In conclusion, understanding the role of methylation in adaptation has been proven challenging, even in the best-studied model organisms (Heckwolf et al, 2020;Hu & Barrett, 2023;Husby, 2022;Kelley et al, 2021;Schmid et al, 2018). Our findings therefore high-…”

Section: Discussionmentioning

confidence: 62%

“…In conclusion, understanding the role of methylation in adaptation has been proven challenging, even in the best‐studied model organisms (Heckwolf et al., 2020; Hu & Barrett, 2023; Husby, 2022; Kelley et al., 2021; Schmid et al., 2018). Our findings therefore highlight the need for additional studies in other ecological model organisms to fully elucidate the role methylation plays in adaptation.…”

Section: Discussionmentioning

confidence: 99%

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DNA methylation differences between stick insect ecotypes

de Carvalho,

Slate,

Villoutreix

et al. 2023

Molecular Ecology

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Epigenetic mechanisms, such as DNA methylation, can influence gene regulation and affect phenotypic variation, raising the possibility that they contribute to ecological adaptation. Beginning to address this issue requires high‐resolution sequencing studies of natural populations to pinpoint epigenetic regions of potential ecological and evolutionary significance. However, such studies are still relatively uncommon, especially in insects, and are mainly restricted to a few model organisms. Here, we characterize patterns of DNA methylation for natural populations of Timema cristinae adapted to two host plant species (i.e. ecotypes). By integrating results from sequencing of whole transcriptomes, genomes and methylomes, we investigate whether environmental, host and genetic differences of these stick insects are associated with methylation levels of cytosine nucleotides in the CpG context. We report an overall genome‐wide methylation level for T. cristinae of ~14%, with methylation being enriched in gene bodies and impoverished in repetitive elements. Genome‐wide DNA methylation variation was strongly positively correlated with genetic distance (relatedness), but also exhibited significant host‐plant effects. Using methylome‐environment association analysis, we pinpointed specific genomic regions that are differentially methylated between ecotypes, with these regions being enriched for genes with functions in membrane processes. The observed association between methylation variation and genetic relatedness, and with the ecologically important variable of host plant, suggests a potential role for epigenetic modification in T. cristinae adaptation. To substantiate such adaptive significance, future studies could test whether methylation can be transmitted across generations and the extent to which it responds to experimental manipulation in field and laboratory studies.

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Section: Discussionmentioning

confidence: 62%

Section: Discussionmentioning

confidence: 99%

DNA methylation differences between stick insect ecotypes

de Carvalho,

Slate,

Villoutreix

et al. 2023

Molecular Ecology

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“…The potential importance of epigenetic mechanisms in mediating plastic responses has long been discussed ( Johnson and Tricker 2010 ) and, more recently, demonstrated experimentally ( Stajic et al 2019 ). Although the environmental induction of a particular epigenetic state (e.g., addition or removal of DNAme) can occur in the context of adaptive mechanisms ( Lämke and Bäurle 2017 ), such an induction may not necessarily constitute an adaptive response (see also Hu and Barrett 2023 ). As such, we considered environmental inducibility in a different context, in that the degree of environmental inducibility of methylation state is (inversely) indicative of the degree of intrinsic regulation.…”

Section: Discussionmentioning

confidence: 99%

High Nucleotide Diversity Accompanies Differential DNA Methylation in Naturally Diverging Populations

Ord

Gossmann²,

Adrian‐Kalchhauser

2023

Molecular Biology and Evolution

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Epigenetic mechanisms such as DNA methylation (DNAme) are thought to comprise an invaluable adaptive toolkit in the early stages of local adaptation, especially when genetic diversity is constrained. However, the link between genetic diversity and DNAme has been scarcely examined in natural populations, despite its potential to shed light on the evolutionary forces acting on methylation state. Here, we analysed reduced-representation bisulfite sequencing and whole genome pool-seq data from marine and freshwater stickleback populations to examine the relationship between DNAme variation (between- and within-population), and nucleotide diversity in the context of freshwater adaptation. We find that sites that are differentially methylated between populations have higher underlying standing genetic variation, with diversity higher among sites that gained methylation in freshwater than those that lost it. Strikingly, while nucleotide diversity is generally lower in the freshwater population as expected from a population bottleneck, this is not the case for sites which lost methylation which instead have elevated nucleotide diversity in freshwater compared to marine. Subsequently, we show that nucleotide diversity is higher among sites with ancestrally variable methylation and also positively correlates with the sensitivity to environmentally induced methylation change. The results suggest that as selection on the control of methylation state becomes relaxed, so too does selection against mutations at the sites themselves. Increased epigenetic variance in a population is therefore likely to precede genetic diversification.

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“…Variations in epigenetic modifications like DNA methylation are important contributors to phenotypic plasticity and evolutionary changes in natural populations (Chapelle & Silvestre, 2022 ; Heckwolf et al., 2020 ; Hu & Barrett, 2022 ; Sagonas et al., 2020 ). Moreover, epigenetic diversity itself may enable and drive adaptation and even speciation (Flores et al., 2013 ; Lamka et al., 2022 ; Vernaz et al., 2022 ; Weiner & Katz, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Epigenetic diversity of genes with copy number variations among natural populations of the three‐spined stickleback

Chain,

Meyer,

Heckwolf

et al. 2024

Evolutionary Applications

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Duplicated genes provide the opportunity for evolutionary novelty and adaptive divergence. In many cases, having more gene copies increases gene expression, which might facilitate adaptation to stressful or novel environments. Conversely, overexpression or misexpression of duplicated genes can be detrimental and subject to negative selection. In this scenario, newly duplicate genes may evade purifying selection if they are epigenetically silenced, at least temporarily, leading them to persist in populations as copy number variations (CNVs). In animals and plants, younger gene duplicates tend to have higher levels of DNA methylation and lower levels of gene expression, suggesting epigenetic regulation could promote the retention of gene duplications via expression repression or silencing. Here, we test the hypothesis that DNA methylation variation coincides with young duplicate genes that are segregating as CNVs in six populations of the three‐spined stickleback that span a salinity gradient from 4 to 30 PSU. Using reduced‐representation bisulfite sequencing, we found DNA methylation and CNV differentiation outliers rarely overlapped. Whereas lineage‐specific genes and young duplicates were found to be highly methylated, just two gene CNVs showed a significant association between promoter methylation level and copy number, suggesting that DNA methylation might not interact with CNVs in our dataset. If most new duplications are regulated for dosage by epigenetic mechanisms, our results do not support a strong contribution from DNA methylation soon after duplication. Instead, our results are consistent with a preference to duplicate genes that are already highly methylated.

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The role of plastic and evolvedDNAmethylation in parallel adaptation of threespine stickleback (Gasterosteus aculeatus)

Cited by 9 publications

References 110 publications

DNA methylation differences between stick insect ecotypes

DNA methylation differences between stick insect ecotypes

High Nucleotide Diversity Accompanies Differential DNA Methylation in Naturally Diverging Populations

Epigenetic diversity of genes with copy number variations among natural populations of the three‐spined stickleback

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