Temporal Dynamics of DNA Methylation Patterns in Response to Rearing Juvenile Steelhead (Oncorhynchus mykiss) in a Hatchery versus Simulated Stream Environment

Abstract

Genetic selection is often implicated as the underlying cause of heritable phenotypic differences between hatchery and wild populations of steelhead trout (Oncorhynchus mykiss) that also differ in lifetime fitness. Developmental plasticity, which can also affect fitness, may be mediated by epigenetic mechanisms such as DNA methylation. Our previous study identified significant differences in DNA methylation between adult hatchery- and natural-origin steelhead from the same population that could not be distinguished by DNA sequence variation. In the current study, we tested whether hatchery-rearing conditions can influence patterns of DNA methylation in steelhead with known genetic backgrounds, and assessed the stability of these changes over time. Eyed-embryos from 22 families of Methow River steelhead were split across traditional hatchery tanks or a simulated stream-rearing environment for 8 months, followed by a second year in a common hatchery tank environment. Family assignments were made using a genetic parentage analysis to account for relatedness among individuals. DNA methylation patterns were examined in the liver, a relatively homogeneous organ that regulates metabolic processes and somatic growth, of juveniles at two time points: after eight months of rearing in either a tank or stream environment and after a subsequent year of rearing in a common tank environment. Further, we analyzed DNA methylation in the sperm of mature 2-year-old males from the earlier described treatments to assess the potential of environmentally-induced changes to be passed to offspring. Hepatic DNA methylation changes in response to hatchery versus stream-rearing in yearling fish were substantial, but few persisted after a second year in the tank environment. However, the early rearing environment appeared to affect how fish responded to developmental and environmental signals during the second year since novel DNA methylation differences were identified in the livers of hatchery versus stream-reared fish after a year of common tank rearing. Furthermore, we found profound differences in DNA methylation due to age, irrespective of rearing treatment. This could be due to smoltification associated changes in liver physiology after the second year of rearing. Although few rearing-treatment effects were observed in the sperm methylome, strong family effects were observed. These data suggest limited potential for intergenerational changes, but highlight the importance of understanding the effects of kinship among studied individuals in order to properly analyze and interpret DNA methylation data in natural populations. Our work is the first to study family effects and temporal dynamics of DNA methylation patterns in response to hatchery-rearing.

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.…”