Strong Parallel Differential Gene Expression Induced by Hatchery Rearing Weakly Associated with Methylation Signals in Adult Coho Salmon (O. kisutch)

Abstract

Human activities and resource exploitation led to a massive decline of wild salmonid populations, consequently numerous conservation programs have been developed to supplement wild populations. However, many studies documented reduced fitness of hatchery-born relative to wild fish. Here, by using both RNA sequencing and Whole Genome Bisulfite Sequencing (WGBS), we show that of hatchery and wild born adult Coho Salmon (Oncorhynchus kisutch) originating from two previously studied river systems, early-life hatchery rearing environment induced significant and parallel gene expression differentiation is maintained until Coho come back to their natal river for reproduction. A total of 3,643 genes differentially expressed and 859 co-expressed genes were down-regulated in parallel in hatchery born fish from both rivers relative to their wild congeners. Among those genes, 26 displayed a significant relationship between gene expression and the median gene body methylation and 669 single CpG displayed a significant correlation between methylation level and the associated gene expression. The link between methylation and gene expression was weak suggesting that DNA methylation is not the only player in mediating hatchery-related expression differences. Yet, significant gene expression differentiation was observed despite 18 month spent in a common environment (i.e. the sea). Finally, the differentiation is observed in parallel in two different river system, highlighting the fact that early life environment may account for at least some of the reduced fitness of the hatchery salmon in the wild. These results illustrate the relevance and importance of considering both epigenome and transcriptome to evaluate the costs and benefits of large-scale supplementation programs.

A global synthesis of peer‐reviewed research on the effects of hatchery salmonids on wild salmonids

“…Christie et al (2016) found a single generation in a hatchery environment altered the expression of over 700 genes in steelhead. Other research has found similar results (Leitwein et al, 2022), even in the absence of genetic differentiation between wild and hatchery populations (Le Luyer et al, 2017), and the potential for the epigenetic changes to be passed along to offspring (Leitwein et al, 2021; Venney et al, 2023). Though the duration of impacts remains unclear it is hypothesized that heritable epigenetic effects may alter the evolutionary trajectory of wild populations, which is a critical issue to evaluate where hatchery salmonids are allowed to or are able to breed with wild salmonids (Skinner & Nilsson, 2021).…”

“…Christie et al (2016) found a single generation in a hatchery environment altered the expression of over 700 genes in steelhead. Other research has found similar results (Leitwein et al, 2022), even in the absence of genetic differentiation between wild and hatchery populations (Le Luyer et al, 2017), and the potential for the epigenetic changes to be passed along to offspring (Leitwein et al, 2021;Venney et al, 2023).…”

Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: sex-specificity and intergenerational stability

“…While the epigenetic effects of hatchery rearing in salmonids are well-documented (Gavery et al, 2019, 2018; Koch et al, 2022; Le Luyer et al, 2017; Leitwein et al, 2021, 2022; Rodriguez Barreto et al, 2019; Venney et al, 2021; Wellband et al, 2021), the long-term stability of these changes after release into natural systems has not been extensively studied, nor has the sex-specificity of the effects of hatchery rearing on the methylome. Here we showed that hatchery rearing led to general and sex-specific changes in Atlantic salmon fin DNA methylation that persisted until the salmon returned to spawn, consistent with similar results in Coho salmon returning to freshwater after eighteen months at sea (Leitwein et al, 2021).…”

“…A single generation of hatchery rearing is generally insufficient to cause genetic differentiation between captive and wild salmon (Gavery, Nichols, Goetz, Middleton, & Swanson, 2018; Le Luyer et al, 2017), though SNPs associated with domestication have been detected after several generations of hatchery rearing in Atlantic salmon (Harder & Christie, 2022). However, the hatchery environment has been shown to induce transcriptional changes in steelhead ( Oncorhynchus mykiss ; Christie, Marine, Fox, French, & Blouin, 2016), Atlantic salmon (Frisk et al, 2020), and Coho salmon ( O. kisutch ; Leitwein et al, 2022). This led to the idea that epigenetic mechanisms controlling gene expression, such as DNA methylation, may serve as the molecular mechanisms underlying rapid phenotypic shifts and fitness declines in hatchery environments.…”

Environment and genotype predict the genomic nature of domestication of salmonids as revealed by gene expression

“…It is difficult to note the extent to which strains within species differ; however, we note no large differences among the five strains of Atlantic salmon for which percentage of genes as DEGs could be calculated, and extensive overlaps between DEGs under domestication is observed where multiple strains are included in a single study [27]. The large estimate of DEGs under domestication in hatchery Coho salmon [47] deserves comment. This was the only study to examine fully sexually mature individuals, and individuals that had completed the at-sea proportion of the anadromous life cycle.…”