DNA Methylation Changes in the Sperm of Captive-Reared Fish: A Route to Epigenetic Introgression in Wild Populations

Abstract

Interbreeding between hatchery-reared and wild fish, through deliberate stocking or escapes from fish farms, can result in rapid phenotypic and gene expression changes in hybrids, but the underlying mechanisms are unknown. We assessed if one generation of captive breeding was sufficient to generate inter- and/or transgenerational epigenetic modifications in Atlantic salmon. We found that the sperm of wild and captive-reared males differed in methylated regions consistent with early epigenetic signatures of domestication. Some of the epigenetic marks that differed between hatchery and wild males affected genes related to transcription, neural development, olfaction, and aggression, and were maintained in the offspring beyond developmental reprogramming. Our findings suggest that rearing in captivity may trigger epigenetic modifications in the sperm of hatchery fish that could explain the rapid phenotypic and genetic changes observed among hybrid fish. Epigenetic introgression via fish sperm represents a previously unappreciated mechanism that could compromise locally adapted fish populations.

Captive-bred Atlantic salmon released into the wild have fewer offspring than wild-bred fish and decrease population productivity

“…This may reflect inadvertent domestication selection, relaxed natural and sexual selection, or epigenetic inheritance. While studies of salmonines are beginning to reveal epigenetic effects of hatchery rearing [19,21], further Table 1. Cohort-and sex-specific, and overall estimates of unbiased RRS for Atlantic salmon.…”

“…Lower LRS in captive-bred fish relative to wild-bred could be explained by reduced survival of their offspring in the wild due to transgenerational effects of the hatchery on offspring phenotypes [20] via genetic [41] or epigenetic inheritance [19]. However, captive-bred fish could simply have lower spawning success [32] or, in the case of females, higher rates of egg retention [49].…”

Environment-driven reprogramming of gamete DNA methylation occurs during maturation and is transmitted intergenerationally in salmon

“…Numerous studies have failed to demonstrate significant genetic difference between hatchery-origin and natural-origin (wild) salmon (Christie et al 2016;Le Luyer et al 2017;Gavery et al 2018) despite documented pronounced differences in gene expression (Christie et al 2016). In contrast, DNA methylation divergence has been reported between hatchery-origin and wild salmon for several species (Le Luyer et al 2017;Gavery et al 2018Gavery et al , 2019; Rodriguez Barreto et al 2019). Evidence for intergenerational effects has recently emerged (Rodriguez Barreto et al 2019), although solely in the context of early-life hatchery exposure.…”

Relative roles of genetic and epigenetic variation on the ecology and evolution of mangrove killifishes (Kryptolebias spp.)

“…These include parental care, cultural transmission, intrauterine environments, which affect offspring fitness without being directly transmitted by the germline cells (Bonduriansky and Day 2009). Although phenotypically-plastic traits have been extensively reported across a wide range of taxa (West-Eberhard 2003), and the evidence for parental effects transmitted via germline cells have been increasingly reported (Chen et al 2016;Illum et al 2018;Posner et al 2019;Rodgers et al 2015;Rodriguez-Barreto et al 2019), the knowledge about the molecular mechanisms in charge of generating and transmitting plastic phenotypes throughout generations is still incipient, as well as their stability and evolutionary role (Dickins and Rahman 2012;Duncan et al 2014;Richards 2006).…”

“…For example, sperm DNA methylation patterns are used as a template for zebrafish (Danio rerio) embryos methylome (Jiang et al 2013). Additional evidence in Atlantic salmon (Salmo salar) has shown that few DNA methylation epialleles induced by domestication escape epigenetic reprogramming and are maintained in the offspring (Rodriguez-Barreto et al 2019).…”