The evolutionary consequences of interactions between the epigenome, the genome and the environment.

The epigenome is the suite of interacting chemical marks and molecules that helps to shape patterns of development, phenotypic plasticity and gene regulation, in part due to its responsiveness to environmental stimuli. There is increasing interest in understanding the functional and evolutionary importance of this sensitivity under ecologically realistic conditions. Observations that epigenetic variation abounds in natural populations have prompted speculation that it may facilitate evolutionary responses to rapid environmental perturbations, such as those occurring under climate change. A frequent point of contention is whether epigenetic variants reflect genetic variation or are independent of it. The genome and epigenome often appear tightly linked and interdependent. While many epigenetic changes are genetically determined, the converse is also true, with DNA sequence changes influenced by the presence of epigenetic marks. Understanding how the epigenome, genome and environment interact with one another is therefore an essential step in explaining the broader evolutionary consequences of epigenomic variation. Drawing on results from experimental and comparative studies carried out in diverse plant and animal species, we synthesize our current understanding of how these factors interact to shape phenotypic variation in natural populations, with a focus on identifying similarities and differences between taxonomic groups. We describe the main components of the epigenome and how they vary within and between taxa. We review how variation in the epigenome interacts with genetic features and environmental determinants, with a focus on the role of transposable elements (TEs) in integrating the epigenome, genome and environment. And we look at recent studies investigating the functional and evolutionary consequences of these interactions. Although epigenetic differentiation in nature is likely often a result of drift or selection on stochastic epimutations, there is growing evidence that a significant fraction of it can be stably inherited and could therefore contribute to evolution independently of genetic change.

DNA methylation in the wild: epigenetic transgenerational inheritance can mediate adaptation in clones of wild strawberry (Fragaria vesca).

Due to the accelerating climate change, it is crucial to understand how plants adapt to rapid environmental changes. Such adaptation may be mediated by epigenetic mechanisms like DNA methylation, which could heritably alter phenotypes without changing the DNA sequence, especially across clonal generations. However, we are still missing robust evidence of the adaptive potential of DNA methylation in wild clonal populations. Here, we studied genetic, epigenetic and transcriptomic variation of Fragaria vesca, a predominantly clonally reproducing herb. We examined samples from 21 natural populations across three climatically distinct geographic regions, as well as clones of the same individuals grown in a common garden. We found that epigenetic variation was partly associated with climate of origin, particularly in non-CG contexts. Importantly, a large proportion of this variation was heritable across clonal generations. Additionally, a subset of these epigenetic changes affected the expression of genes mainly involved in plant growth and responses to pathogen and abiotic stress. These findings highlight the potential influence of epigenetic changes on phenotypic traits. Our findings indicate that variation in DNA methylation, which can be environmentally inducible and heritable, may enable clonal plant populations to adjust to their environmental conditions even in the absence of genetic adaptation.

Response of Fragaria vesca to projected change in temperature, water availability and concentration of CO2 in the atmosphere.

The high rate of climate change may soon expose plants to conditions beyond their adaptation limits. Clonal plants might be particularly affected due to limited genotypic diversity of their populations, potentially decreasing their adaptability. We therefore tested the ability of a widely distributed predominantly clonally reproducing herb (Fragaria vesca) to cope with periods of drought and flooding in climatic conditions predicted to occur at the end of the twenty-first century, i.e. on average 4 °C warmer and with twice the concentration of CO2 in the air (800 ppm) than the current state. We found that F. vesca can phenotypically adjust to future climatic conditions, although its drought resistance may be reduced. Increased temperature and CO2 levels in the air had a far greater effect on growth, phenology, reproduction, and gene expression than the temperature increase itself, and promoted resistance of F. vesca to repeated flooding periods. Higher temperature promoted clonal over sexual reproduction, and increased temperature and CO2 concentration in the air triggered change in expression of genes controlling the level of self-pollination. We conclude that F. vesca can acclimatise to predicted climate change, but the increased ratio of clonal to sexual reproduction and the alteration of genes involved in the self-(in)compatibility system may be associated with reduced genotypic diversity of its populations, which may negatively impact its ability to genetically adapt to novel climate in the long-term.

Epigenetic targeting of transposon relics: beating the dead horses of the genome?

Transposable elements (TEs) have been seen as selfish genetic elements that can propagate in a host genome. Their propagation success is however hindered by a combination of mechanisms such as mutations, selection, and their epigenetic silencing by the host genome. As a result, most copies of TEs in a given genome are dead relics: their sequence is too degenerated to allow any transposition. Nevertheless, these TE relics often, but not always, remain epigenetically silenced, and if not to prevent transposition anymore, one can wonder the reason for this phenomenon. The mere self-perpetuating loop inherent to epigenetic silencing could alone explain that even when inactive, TE copies remain silenced. Beyond this process, nevertheless, antagonistic selective forces are likely to act on TE relic silencing. Especially, without the benefit of preventing transposition, TE relic silencing may prove deleterious to the host fitness, suggesting that the maintenance of TE relic silencing is the result of a fine, and perhaps case-by-case, evolutionary trade-off between beneficial and deleterious effects. Ultimately, the release of TE relics silencing may provide a 'safe' ground for adaptive epimutations to arise. In this review, we provide an overview of these questions in both plants and animals.

DNA Methylation Can Mediate Local Adaptation and Response to Climate Change in the Clonal Plant Fragaria vesca: Evidence From a European-Scale Reciprocal Transplant Experiment.

The ongoing climate crisis represents a growing threat for plants and other organisms. However, how and if plants will be able to adapt to future environmental conditions is still debated. One of the most powerful mechanisms allowing plants to tackle the changing climate is phenotypic plasticity, which can be regulated by epigenetic mechanisms. Environmentally induced epigenetic variation mediating phenotypic plasticity might be heritable across (a)sexual generations, thus potentially enabling rapid adaptation to climate change. Here, we assessed whether epigenetic mechanisms, DNA methylation in particular, enable for local adaptation and response to increased and/or decreased temperature of natural populations of a clonal plant, Fragaria vesca (wild strawberry). We collected ramets from three populations along a temperature gradient in each of three countries covering the southern (Italy), central (Czechia), and northern (Norway) edges of the native European range of F. vesca. After clonal propagation and alteration of DNA methylation status of half of the plants via 5-azacytidine, we reciprocally transplanted clones to their home locality and to the other two climatically distinct localities within the country of their origin. At the end of the growing season, we recorded survival and aboveground biomass as fitness estimates. We found evidence for local adaptation in intermediate and cold populations in Italy and maladaptation of plants of the warmest populations in all countries. Plants treated with 5-azacytidine showed either better or worse performance in their local conditions than untreated plants. Application of 5-azacytidine also affected plant response to changed climatic conditions when transplanted to the colder or warmer locality than was their origin, and the response was, however, country-specific. We conclude that the increasing temperature will probably be the limiting factor determining F. vesca survival and distribution. DNA methylation may contribute to local adaptation and response to climatic change in natural ecosystems; however, its role may depend on the specific environmental conditions. Since adaptation mediated by epigenetic variation may occur faster than via natural selection on genetic variants, epigenetic adaptation might to some degree help plants in keeping up with the ongoing environmental crisis.