Epigenetics in teleost fish: From molecular mechanisms to physiological phenotypes

Abstract

While the field of epigenetics is increasingly recognized to contribute to the emergence of phenotypes in mammalian research models across different developmental and generational timescales, the comparative biology of epigenetics in the large and physiologically diverse vertebrate infraclass of teleost fish remains comparatively understudied. The cypriniform zebrafish and the salmoniform rainbow trout and Atlantic salmon represent two especially important teleost orders, because they offer the unique possibility to comparatively investigate the role of epigenetic regulation in 3R and 4R duplicated genomes. In addition to their sequenced genomes, these teleost species are well-characterized model species for development and physiology, and therefore allow for an investigation of the role of epigenetic modifications in the emergence of physiological phenotypes during an organism's lifespan and in subsequent generations. This review aims firstly to describe the evolution of the repertoire of genes involved in key molecular epigenetic pathways including histone modifications, DNA methylation and microRNAs in zebrafish, rainbow trout, and Atlantic salmon, and secondly, to discuss recent advances in research highlighting a role for molecular epigenetics in shaping physiological phenotypes in these and other teleost models. Finally, by discussing themes and current limitations of the emerging field of teleost epigenetics from both theoretical and technical points of view, we will highlight future research needs and discuss how epigenetics will not only help address basic research questions in comparative teleost physiology, but also inform translational research including aquaculture, aquatic toxicology, and human disease.

Atlantic salmon (Salmo salar L.) genetics in the 21st century: taking leaps forward in aquaculture and biological understanding

“…The epigenetic molecular component of phenotypic variability in salmonids is relatively poorly understood but holds promise for translational research relevant to stock enhancement in aquaculture (for recent reviews, see Gavery & Roberts ; Best et al . ). In this respect, FAASG aims to exploit a range of well‐established technologies that enable profiling of DNA methylation, repressive and permissive histone modifications, chromatin accessibility and higher chromatin structure (Macqueen et al .…”

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems

“…Recent epigenetics studies have focused mostly on stable heritable phenotypes that result from structural changes in chromatin (e.g. DNA methylation or histone modification) without alternations in the DNA nucleotide sequence itself (Berger et al ., ; Best et al ., ). Although these changes can be self‐perpetuated over generations by the phenotypic outcome of epigenetic responses (Flores, Wolschin, & Amdam, ), some environmentally induced epigenetic modifications are repeatable across similar environments (Le Luyer et al ., ) and stably inherited across generations (Danchin, ).…”

“…Although these changes can be self‐perpetuated over generations by the phenotypic outcome of epigenetic responses (Flores, Wolschin, & Amdam, ), some environmentally induced epigenetic modifications are repeatable across similar environments (Le Luyer et al ., ) and stably inherited across generations (Danchin, ). Recent studies have identified differentially methylated regions associated with adaptive phenotypic variation in postglacial fishes (Best et al ., ), such as lateral plate morphs in three‐spined stickleback (Smith et al ., ), migration phenotypes in rainbow trout ( Oncorhynchus mykiss ) (Baerwald et al ., ) and the degree of behavioural reproductive isolation in tessellated darters ( Etheostoma olmstedi ) (Smith et al ., ). However, the frequency with which environmentally induced epigenetic variation is inherited is currently unknown (Smith & Ritchie, ) and we need to understand how stable heritable phenotypes that result from structural changes in chromatin may feed back to, and influence, genetic variation, ecology, and evolution.…”

Stearoyl-CoA desaturase (scd1a) is epigenetically regulated by broodstock nutrition in gilthead sea bream (Sparus aurata)

“…However, such a clear association remains elusive in non-model fish species [46]. Moreover, most studies in marine fish, including those conducted in gilthead sea bream, have managed the ratio n-3-LC-PUFA/C18 PUFA, but have not yet consider the potential value of C18 PUFA alone as a nutritional programing tool [40,41,42].…”