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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 of hatchery and wild-born adult Coho salmon (Oncorhynchus kisutch) originating from two previously studied river systems, we show that 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 coexpressed genes were downregulated 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 CpGs 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 months spent in a common environment (i.e. the sea). Finally, the differentiation is observed in parallel in two different river systems, 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. [ABSTRACT FROM AUTHOR]

Human activities induce direct or indirect selection pressure on natural population and may ultimately affect population's integrity. While numerous conservation programs aimed to minimize human‐induced genomic variation, human‐induced environmental variation may generate epigenomic variation potentially affecting fitness through phenotypic modifications. Major questions remain pertaining to how much epigenomic variation arises from environmental heterogeneity, whether this variation can persist throughout life, and whether it can be transmitted across generations. We performed whole genome bisulfite sequencing (WGBS) on the sperm of genetically indistinguishable hatchery and wild‐born migrating adults of Coho salmon (Oncorhynchus kisutch) from two geographically distant rivers at different epigenome scales. Our results showed that coupling WGBS with fine‐scale analyses (local and chromosomal) allows the detection of parallel early‐life hatchery‐induced epimarks that differentiate wild from hatchery‐reared salmon. Four chromosomes and 183 differentially methylated regions (DMRs) displayed a significant signal of methylation differentiation between hatchery and wild‐born Coho salmon. Moreover, those early‐life epimarks persisted in germ line cells despite about 1.5 year spent in the ocean following release from hatchery, opening the possibility for transgenerational inheritance. Our results strengthen the hypothesis that epigenomic modifications environmentally induced during early‐life development persist in germ cells of adults until reproduction, which could potentially impact their fitness. [ABSTRACT FROM AUTHOR]