The implications for aquaculture practice of epigenomic programming of components of the endocrine system of teleostean embryos: lessons learned from mammalian studies

Abstract

Epigenetics is the study of changes in gene expression patterns that occur without any modification of the underlying nucleotide sequence of the DNA. Modifications of the so‐called epigenome include complex transient or permanent chemical changes of the DNA or histone proteins resulting in the suppression or enhancement of gene expression, together with an array of post‐translational events that modify the translational products. Epigenomic programming (EP) of the genome is an essential component of embryonic development in animals from the totipotent fertilized egg to the pluripotent stem cells, stem cell differentiation and final tissue and organ formation. Many of these EP processes are influenced transiently and some permanently by environmental influences. In eutherian mammals, environmentally related EP of embryos is linked to permanent changes in the phenotype of the progeny, some of which have been associated with adult onset metabolic disorders. Moreover, because some of the epigenetic remodelling occurs in both the soma and germ line, the resultant phenotypic characteristics (some of which are linked to disease states) may be heritable. Although far less is known about the effects of environmentally linked EP on the ontogeny of fishes, the available information suggests that the EP processes are similar amongst all vertebrates, and there are clear parallels between fish and mammals that are discussed in this paper. Our perspective takes the well‐established findings in mammals and uses them to proactively extrapolate to the as yet under‐recognized implications of EP for fish biology and for fish production in intensive aquaculture.

Population genomic analyses of early‐phase Atlantic Salmon (Salmo salar) domestication/captive breeding

“…). It has been suggested that environmental stimuli may induce epigenetic changes, which in turn can affect gene expression patterns in novel environments (Li and Leatherland ). It is thus possible that alternative molecular mechanisms, such as gene expression tuning (Roberge et al.…”

Does maternal captivity of wild, migratory sockeye salmon influence offspring performance?

“…Thus, other components of the egg such as thyroid or sex steroid hormones (de Jesus & Hirano, 1992) or microRNA (Ma et al, 2015) may be causing the observed differences in offspring. Epigenetic programming is an established mechanism of intergenerational change in mammals (reviewed in Dunn et al, 2011), and emerging as a candidate mechanism in oviparous taxa as well (Lindqvist et al, 2007;Li & Leatherland, 2013). Continued exploration and methodological refinement of assessing changes to gamete and offspring epigenome in fish is warranted.…”

Using parentage analysis to estimate rates of straying and homing in Chinook salmon (Oncorhynchus tshawytscha)

“…; Jonsson & Jonsson ). In a recent review, Li & Leatherland () concluded that hatchery rearing might be expected to have an influence on epigenetic programming, particularly of genes related to endocrine processes. Such processes are known to be critical to juvenile imprinting in salmon, and altered hormone profiles have been suggested to lead to increased straying of hatchery‐origin fish (reviewed by Keefer & Caudill ).…”