Environmental Change-Dependent Inherited Epigenetic Response

Abstract

Epigenetic modifications are a mechanism conveying environmental information to subsequent generations via parental germ lines. Research on epigenetic responses to environmental changes in wild mammals has been widely neglected, as well as studies that compare responses to changes in different environmental factors. Here, we focused on the transmission of DNA methylation changes to naive male offspring after paternal exposure to either diet (~40% less protein) or temperature increase (10 °C increased temperature). Because both experiments focused on the liver as the main metabolic and thermoregulation organ, we were able to decipher if epigenetic changes differed in response to different environmental changes. Reduced representation bisulfite sequencing (RRBS) revealed differentially methylated regions (DMRs) in annotated genomic regions in sons sired before (control) and after the fathers’ treatments. We detected both a highly specific epigenetic response dependent on the environmental factor that had changed that was reflected in genes involved in specific metabolic pathways, and a more general response to changes in outer stimuli reflected by epigenetic modifications in a small subset of genes shared between both responses. Our results indicated that fathers prepared their offspring for specific environmental changes by paternally inherited epigenetic modifications, suggesting a strong paternal contribution to adaptive processes.

The Epigenetics Dilemma

“…As a consequence, results presented in this issue and elsewhere make clear that this is a time of opportunity for epigenetics as its contours and impact are traced more and more clearly: the epigenome is demonstrated to be very plastic, it changes during development [2], but also, and in a different way, when exposed to external environmental cues. These changes occur sometimes within generations [3] and, in other cases, epigenetic plasticity occurs through generations [4,5], conveying parental effects of very different type (e.g., parental diet or hatchery environment).However, this plastic character of the epigenome makes it also difficult to draw general conclusions on how every epigenotype, genotype and phenotype are interrelated. In this issue, it is shown that phenotypic, and thus potentially gene expression changes, can precede epigenetic changes [3], or that they occur after the initial environmental stimulus [4,5].…”

“…These changes occur sometimes within generations [3] and, in other cases, epigenetic plasticity occurs through generations [4,5], conveying parental effects of very different type (e.g., parental diet or hatchery environment).However, this plastic character of the epigenome makes it also difficult to draw general conclusions on how every epigenotype, genotype and phenotype are interrelated. In this issue, it is shown that phenotypic, and thus potentially gene expression changes, can precede epigenetic changes [3], or that they occur after the initial environmental stimulus [4,5]. It is also shown that epigenetic modifications can be associated with the magnitude of change in reaction norms of some but not all phenotypic traits [6].…”

“…As a consequence, results presented in this issue and elsewhere make clear that this is a time of opportunity for epigenetics as its contours and impact are traced more and more clearly: the epigenome is demonstrated to be very plastic, it changes during development [2], but also, and in a different way, when exposed to external environmental cues. These changes occur sometimes within generations [3] and, in other cases, epigenetic plasticity occurs through generations [4,5], conveying parental effects of very different type (e.g., parental diet or hatchery environment).…”

“…It is also shown that epigenetic modifications can be associated with the magnitude of change in reaction norms of some but not all phenotypic traits [6]. In addition, even when considering the same bearer of epigenetic information (e.g., DNA methylation), different organisms show different types of DNA methylation (e.g., [1][2][3][4][5][6]) with potentially different types of phenotypic effects. Nevertheless, epigenetic changes do not occur randomly along the genome.…”

“…Nevertheless, epigenetic changes do not occur randomly along the genome. In the two examples presented in this issue, environmentally induced epimutations were clearly enriched in the pathways of alert information and signaling: between 40% [5] and 66% [4] of differentially methylated regions (DMR) occurred in genes associated with signal transduction. This suggests that DMR are involved in the management of enduring and adequate stress response information.…”