DNA Methylation Patterns in the Round Goby Hypothalamus Support an On-The-Spot Decision Scenario for Territorial Behavior

Abstract

The question as to how early life experiences are stored on a molecular level and affect traits later in life is highly topical in ecology, medicine, and epigenetics. In this study, we use a fish model to investigate whether DNA methylation mediates early life experiences and predetermines a territorial male reproductive phenotype. In fish, adult reproductive phenotypes frequently depend on previous life experiences and are often associated with distinct morphological traits. DNA methylation is an epigenetic mechanism which is both sensitive to environmental conditions and stably inherited across cell divisions. We therefore investigate early life predisposition in the round goby Neogobius melanostomus by growth back-calculations and then study DNA methylation by MBD-Seq in the brain region controlling vertebrate reproductive behavior, the hypothalamus. We find a link between the territorial reproductive phenotype and high growth rates in the first year of life. However, hypothalamic DNA methylation patterns reflect the current behavioral status independently of early life experiences. Together, our data suggest a non-predetermination scenario in the round goby, in which indeterminate males progress to a non-territorial status in the spawning season, and in which some males then assume a specialized territorial phenotype if current conditions are favorable.

The round goby genome provides insights into mechanisms that may facilitate biological invasions

“…Web of Science records on round goby (orange) have risen since its first detection in the Great Lakes in contrast to records on a non-invasive fish with similar ecology (European bullhead, Cottus gobio; gray) methylating PRC2 complex and the DNA methylases. Both mechanisms are implicated in the regulation of developmental plasticity and gene expression and have been linked to plastic responses, behavioral changes, and environmental memory [51][52][53][54][55].…”

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.…”