Characterization of Genetic and Epigenetic Variation in Sperm and Red Blood Cells from Adult Hatchery and Natural-Origin Steelhead, Oncorhynchus mykiss

Abstract

While the goal of most conservation hatchery programs is to produce fish that are genetically and phenotypically indistinguishable from the wild stocks they aim to restore, there is considerable evidence that salmon and steelhead reared in hatcheries differ from wild fish in phenotypic traits related to fitness. Some evidence suggests that these phenotypic differences have a genetic basis (e.g., domestication selection) but another likely mechanism that remains largely unexplored is that differences between hatchery and wild populations arise as a result of environmentally-induced heritable epigenetic change. As a first step toward understanding the potential contribution of these two possible mechanisms, we describe genetic and epigenetic variation in hatchery and natural-origin adult steelhead, Oncorhynchus mykiss, from the Methow River, WA. Our main objectives were to determine if hatchery and natural-origin fish could be distinguished genetically and whether differences in epigenetic programming (DNA methylation) in somatic and germ cells could be detected between the two groups. Genetic analysis of 72 fish using 936 SNPs generated by Restriction Site Associated DNA Sequencing (RAD-Seq) did not reveal differentiation between hatchery and natural-origin fish at a population level. We performed Reduced Representation Bisulfite Sequencing (RRBS) on a subset of 10 hatchery and 10 natural-origin fish and report the first genome-wide characterization of somatic (red blood cells (RBCs)) and germ line (sperm) derived DNA methylomes in a salmonid, from which we identified considerable tissue-specific methylation. We identified 85 differentially methylated regions (DMRs) in RBCs and 108 DMRs in sperm of steelhead reared for their first year in a hatchery environment compared to those reared in the wild. This work provides support that epigenetic mechanisms may serve as a link between hatchery rearing and adult phenotype in steelhead; furthermore, DMRs identified in germ cells (sperm) highlight the potential for these changes to be passed on to future generations.

Genome-Wide Epigenomic Stress Response in the European Sea Bass (Dicentrarchus Labrax, L.)

“…This indicated slightly more matches with the brain than with other organs investigated so far. However, the single previous study analyzing RBC methylome in sh so far [41] shared no DMC-related gene with the present study. Finally, the study that reported the largest number of genes also found as DMC-related genes in sea bass (n =15) was by Gavery et al [45]; These authors were interested in the liver of hatchery vs wild rainbow trout during a so-called 'temporal analysis' (see Additional File 5).…”

“…The mapping e ciency was high (74.5%) when compared to early values retrieved in human (~65%) [112], or in some recent sh studies screening for genome-wide methylation (e.g. 55-60% in [59]; 40% in [41]). Other studies reported similar mapping e ciencies, but reported percentages of mapping for unique best hits that were generally lower.…”

“…The use of RBCs in sh transcriptomics or proteomics has received attention over the last decade [38][39][40]. However, sh epigenetics has not embarked on this path yet and genome-wide epigenetic studies using RBCs are quite rare in sh [41]. This contrasts with the over-increasing interest to investigate epigenomic variation in teleosts Nevertheless, documenting the epigenomics of the stress axis/network also remains scarce [58], while authors asked for greater attention on this topic [73,74].…”

Anadromy, potamodromy and residency in brown trout Salmo trutta: the role of genes and the environment

“…Many differentially methylated regions (DMR) have been shown to occur in the sperm of hatchery‐reared v . wild O. mykiss , demonstrating the potential for inheritance (Gavery et al ., ). It should be noted that epigenetic inheritance, for example mediated via effects of temperature on gene regulation, could potentially influence the life‐history traits of offspring and perhaps grand‐offspring, irrespective of energy status (Jonsson & Jonsson, ).…”

Supportive breeders of Atlantic salmon Salmo salar have reduced fitness in nature

“…The differentially methylated regions exhibited enrichment for biological functions that may influence migratory and reproductive capacities of the fish and may affect the capacity of hatchery‐born coho salmon to spawn successfully in nature. Also, in steelhead trout, hatcheries induce epigenetic changes as reported by Garvey, Nichols, Goetz, Middleton, and Swanson (). They found differences in several methylated regions in red blood cells and sperm cells between hatchery and wild conspecifics.…”