Epigenetic inheritance and reproductive mode in plants and animals

Anastasiadi, Dafni; Venney, Clare J; Bernatchez, Louis; Wellenreuther, Maren

doi:10.1016/j.tree.2021.08.006

Cited by 82 publications

(111 citation statements)

References 136 publications

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“…The copyright holder for this preprint this version posted February 27, 2022. ; https://doi.org/10.1101/2022.02.25.481661 doi: bioRxiv preprint plantain, and our study on brook charr), consistent with findings that reproductive mode likely influences the prevalence and persistence of epigenetic inheritance [22]. Since epigenetic variation can persist late into the lifespan of offspring and can be transmitted for multiple generations, inheritance in the absence of offspring plasticity can have profound impacts on phenotype and fitness for generations to come [22,76]. The considerable effects of adult sexual maturation temperature on brook charr offspring methylation reported, coupled with the lack of plasticity in DNA methylation due to offspring temperature, could have significant long-term implications for brook charr populations responding to climate change if offspring cannot override inherited epigenetic marks.…”

Section: Discussionsupporting

confidence: 89%

Section: Discussionsupporting

confidence: 88%

“…Epigenetic inheritance refers to the transmission of epigenetic marks (e.g., DNA methylation) from parent to progeny that can modify offspring gene expression, phenotype, and fitness [22,23]. DNA methylation is an important regulator of transcription and has been shown to change in response to temperature [24][25][26][27], differences in rearing environment [28,29], and other factors.…”

Section: Introductionmentioning

confidence: 99%

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Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)

Venney

Wellband

Normandeau

et al. 2022

Preprint

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Epigenetic inheritance can result in plastic responses to changing environments being faithfully transmitted to offspring. However, it remains unclear how epigenetic mechanisms such as DNA methylation can contribute to multigenerational acclimation and adaptation to environmental stressors. Brook charr (Salvelinus fontinalis), an economically important salmonid, is highly sensitive to thermal stress, and is of conservation concern in the context of climate change. We studied the effects of temperature during parental sexual maturation and offspring rearing on whole-genome DNA methylation in brook charr juveniles (fry). Parents were split between warm and cold temperatures during sexual maturation, mated in controlled breeding designs, then offspring from each family were split between warm (8°C) and cold (5°C) rearing environments. We found 188 differentially methylated regions (DMRs) due to parental maturation temperature after controlling for family structure. In contrast, offspring rearing temperature had a negligible effect on offspring methylation. Stable intergenerational inheritance of DNA methylation and minimal plasticity in progeny could result in transmission of acclimatory epigenetic states to offspring, priming them for a warming environment. Our findings have implications pertaining to the role of intergenerational epigenetic inheritance in response to ongoing climate change.

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Section: Discussionsupporting

confidence: 89%

Section: Discussionsupporting

confidence: 88%

Section: Introductionmentioning

confidence: 99%

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Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)

Venney

Wellband

Normandeau

et al. 2022

Preprint

Self Cite

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“…For example, if members of a species possess the capacity for high phenotypic plasticity via environment-induced epigenetic modifications, and these changes generally support survival in novel conditions, then the capacity for epigenetic response can be said to be beneficial even if relevant epigenetic states are not inherited through the germline. Emerging examples do suggest that some environment-induced epigenetic changes can be transmitted across generations, which has been recently reviewed (Anastasiadi et al, 2021).…”

Section: Adaptive Potential and Response To Environmental Changementioning

confidence: 99%

Epigenomics as a paradigm to understand the nuances of phenotypes

Fanter

Madelaire

Genereux

et al. 2022

Journal of Experimental Biology

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Quantifying the relative importance of genomic and epigenomic modulators of phenotype is a focal challenge in comparative physiology, but progress is constrained by availability of data and analytic methods. Previous studies have linked physiological features to coding DNA sequence, regulatory DNA sequence, and epigenetic state, but few have disentangled their relative contributions or unambiguously distinguished causative effects (‘drivers’) from correlations. Progress has been limited by several factors, including the classical approach of treating continuous and fluid phenotypes as discrete and static across time and environment, and difficulty in considering the full diversity of mechanisms that can modulate phenotype, such as gene accessibility, transcription, mRNA processing and translation. We argue that attention to phenotype nuance, progressing to association with epigenetic marks and then causal analyses of the epigenetic mechanism, will enable clearer evaluation of the evolutionary path. This would underlie an essential paradigm shift, and power the search for links between genomic and epigenomic features and physiology. Here, we review the growing knowledge base of gene-regulatory mechanisms and describe their links to phenotype, proposing strategies to address widely recognized challenges.

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“…Such eco-evolutionary dynamics may be fundamentally altered if environmentally induced responses are inherited, for example, via epigenetic mechanisms [17]. However, the extent and specificity of transgenerational persistence of environmentally induced epigenetic variation remains poorly understood, not only in Daphnia but in ecological model systems in general [18,19].…”

Section: Introductionmentioning

confidence: 99%

Environmentally-induced DNA methylation is inherited across generations in an aquatic keystone species (Daphnia magna)

Feiner

Radersma

Vasquez

et al. 2021

Preprint

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Environmental stress can result in epigenetic modifications that are passed down several generations. Such epigenetic inheritance can have significant impact on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. Here, we used whole-genome bisulfite sequencing on individual water fleas (Daphnia magna) to assess whether environmentally-induced DNA methylation can persist for up to four generations. Genetically identical females were exposed to a control treatment, one of three natural stressors (high temperature, zinc, microcystin), or the methylation-inhibitor 5-azacytidine. After exposure, lines were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) between controls and F1 individuals whose mothers (and therefore they themselves as germ cells) were exposed to one of the three natural stressors. Between 46% and 58% of these environmentally-induced DMPs persisted until generation F4 without attenuation in their magnitude of differential methylation. DMPs were enriched in exons and largely stressor-specific, suggesting a possible role in environment-dependent gene regulation. In contrast, treatment with the compound 5-azacytidine demonstrated that pervasive hypo-methylation upon exposure is reset almost completely after a single generation. These results suggest that environmentally-induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of fresh-water communities.Author summaryWater fleas are important keystone species mediating eco-evolutionary dynamics in lakes and ponds. It is currently an open question in how far epigenetic inheritance contributes to the ability of Daphnia populations to adapt to environmental stress. Using a range of naturally occurring stressors and a multi-generational design, we show that environmentally-induced DNA methylation variants are stably inherited for at least four generations in Daphnia magna. The induced variation in DNA methylation are stressor-specific and almost exclusively found in exons, bearing the signatures of functional adaptations. Our findings imply that ecological adaptations of Daphnia to seasonal fluctuations can be underpinned by epigenetic inheritance of DNA methylation without changes in gene frequencies.

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Epigenetic inheritance and reproductive mode in plants and animals

Cited by 82 publications

References 136 publications

Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)

Thermal regime during parental sexual maturation, but not during offspring rearing, modulates DNA methylation in brook charr (Salvelinus fontinalis)

Epigenomics as a paradigm to understand the nuances of phenotypes

Environmentally-induced DNA methylation is inherited across generations in an aquatic keystone species (Daphnia magna)

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