Evolutionary consequences of epigenetic inheritance

Lind, Martin I.; Spagopoulou, Foteini

doi:10.1038/s41437-018-0113-y

Cited by 132 publications

(105 citation statements)

References 26 publications

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“…The role of epigenetic variation in governing adaptive evolution remains controversial, yet a growing body of literature demonstrates the ubiquity of transgenerational epigenetic transmission, and consequently considers it as a key evolutionary force (Gugger et al . 2016; Miska & Ferguson-Smith 2016; Lind & Spagopoulou 2018; Schmid et al . 2018; Zhang et al .…”

Section: Introductionmentioning

confidence: 99%

Ecological divergence of DNA methylation patterns at distinct spatial scales

Kort

Panis

Deforce

et al. 2019

Preprint

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Adaptive trait divergence between populations is regulated by genetic and non-genetic processes. Compared to genetic change, epigenetic change is unstable and short-lived, questioning its contribution to long-term adaptive potential. However, epigenetic change can accumulate over time, and may result in beneficial epigenetic memories where environments are heterogeneous. Diverging epigenetic memories have been observed across large spatial scales, and can persist through multiple generations even in the absence of the causative environmental stressor. It is unknown, however, how and to what extent epigenetic memories contribute to fine-scale population structure and evolution. Here, we performed whole genome bisulfite sequencing on 30 Fragaria vesca F1 plants originating from distinct ecological settings and grown in a controlled environment. Specifically, we compared methylation patterns between a steep, altitudinal gradient (<2 km) and a wide spatial gradient (>500 km). If epigenetic variation is random, arising from errors during replication and without evolutionary implications, one would expect similar amounts of epigenetic variation across populations and no spatial scale-effect. Here, we find that epigenetic memories arise even at fine spatial scale, and that both parallel and non-parallel biological processes underpin epigenetic divergence at distinct spatial scales. For example, demethylation of transposable elements consistently occurred at the large but not the small spatial scale, while methylation differentiation for most biological processes were shared between spatial scales. Acute drought stress did not result in significant epigenetic differentiation, indicating that repeated historical stress levels associated with heterogeneous environmental conditions are required for acquiring a stable epigenetic memory and for coping with future environmental change.

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Section: Introductionmentioning

confidence: 99%

Ecological divergence of DNA methylation patterns at distinct spatial scales

Kort

Panis

Deforce

et al. 2019

Preprint

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“…The flexible control of gene expression provided by mechanisms such as DNA methylation has 78 also caught the interest of biologists interested in the underlying mechanisms of phenotypic plasticity, 79 and how such plasticity may evolve Day 2009, 2018). Moreover, there has also 80 been great interest in the extent to which epigenetic modifications may be inherited across 81 generations (Bonduriansky and Day 2009, Burggren 2016, Lind and Spagopoulou 2018. Transmission 82 of epigenetic state allows transmission of parent-of-origin information, or so-called genomic 83 imprinting, setting the scene for genomic conflict (Haig 2002, Patten et al 2014).…”

Section: Introduction 52mentioning

confidence: 99%

Genome-wide disruption of DNA methylation by 5-aza-2’-deoxycytidine in the parasitoid waspNasonia vitripennis

Cook¹,

Parker

Turner

et al. 2018

Preprint

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25DNA methylation of cytosine residues across the genome influences how many genes and phenotypes 26 are regulated. As such, understanding the role of DNA methylation and other epigenetic mechanisms 27 has become very much a part of mapping genotype to phenotype, a major question in evolutionary 28 biology. Ideally, we would like to manipulate DNA methylation patterns on a genome-wide scale, to 29 elucidate the role of epigenetic modifications in phenotypic expression. Recently, the demethylating 30 agent 5-aza-2'-deoxycytidine (5-aza-dC; commonly used in the epigenetic treatment of certain 31 cancers), has been deployed to explore the epigenetic regulation of a number of traits of interest to 32 evolutionary ecologists. Recently, we showed that treatment with 5-aza-dC shifted patterns of sex 33 allocation as predicted by genomic conflict theory in the parasitoid wasp Nasonia vitripennis. This was 34 the first (albeit indirect) experimental evidence for genomic conflict over sex allocation facilitated by 35 DNA methylation. However, this work lacked confirmation of the effects of 5-aza-dC on DNA 36 methylation, drawing commentary on the efficacy of 5-aza-dC in a novel system. Here, using whole-37 genome bisulphite sequencing, we demonstrate unequivocally that 5-aza-dC disrupts methylation 38 across the Nasonia vitripennis genome. We show that disruption leads to both hypo-and hyper-39 methylation, may vary across tissues and time of sampling, and that the effects of 5-aza-dC are 40 context-and sequence specific. We conclude that 5-aza-dC has the potential to be repurposed as a 41 tool in evolutionary ecology for studying the role of DNA methylation. 42 43 44 45 46 47 48 49 50 51

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“…Storey, 2015), it may be assumed that the effect is caused by epigenetic inheritance resulting from epigenetic mechanisms enabling response to environmental cues and stresses as well as passing on of the acquired modulations to the offspring (e.g. Lind & Spagopoulou, 2018).…”

Section: What Is the Impact Of Anhydrobiosis On Individual Fitness?mentioning

confidence: 99%

Staying young and fit? Ontogenetic and phylogenetic consequences of animal anhydrobiosis

et al. 2019

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Although gradual deterioration of life functions with age is not a fundamental rule, it is pervasive among living organisms, regardless of their mode of reproduction and the number of constituent cells. However, deterioration can be temporarily arrested or slowed down due to the process of anhydrobiosis. Two modes of anhydrobiosis can be distinguished for the developmental and adult stages of animals. Developmental resting stages are reported for different animals, including sponges (Porifera), stingers (Cnidaria), flatworms (Platyhelminthes), insects (Insecta), copepods (Copepoda) and branchiopods (Branchiopoda). However, anhydrobiosis occurring at any stage of animal life, including adults, is found only in a few invertebrate phyla, namely roundworms (Nematoda), wheel animals (Rotifera) and water bears (Tardigrada). Notably, in the second group anhydrobiosis has been proposed to eliminate or slow‐down aging symptoms. This, in turn, may correlate with higher fitness and fecundity, and increased offspring longevity. We present available data concerning anhydrobiosis of tardigrades, bdelloid rotifers and nematodes, the only animals known to be capable of anhydrobiosis as adult individuals. The impact of anhydrobiosis on animal aging is illustrated by two models based on experimental data, namely the “Sleeping Beauty” and “Picture of Dorian Grey” models. According to the “Sleeping Beauty” model, anhydrobiotic organisms do not age during anhydrobiosis, whereas the “Picture of Dorian Grey” model predicts that the anhydrobiotic organism ages, at least during the initial stage of anhydrobiosis. Finally, we discuss possible implications of these models for individual longevity and survival as well as phenotypic diversity of taxa and their evolution. A better understanding of life strategies of anhydrobiotic animals both at the ontogenetic and phylogenetic levels can provide answers to many fundamental questions and useful practical outputs in branches of applied sciences.

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Evolutionary consequences of epigenetic inheritance

Cited by 132 publications

References 26 publications

Ecological divergence of DNA methylation patterns at distinct spatial scales

Ecological divergence of DNA methylation patterns at distinct spatial scales

Genome-wide disruption of DNA methylation by 5-aza-2’-deoxycytidine in the parasitoid waspNasonia vitripennis

Staying young and fit? Ontogenetic and phylogenetic consequences of animal anhydrobiosis

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