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.

Keywords: Salmo salar; epigenetic inheritance; DNA methylation; domestication.

Fig. 1

Outline of the experimental design. Parental origin of wild (W) and hatchery (H1 and H2) groups and their offspring. Wild adult salmon were captured from the river Allier on their return to the spawning grounds, H1 salmon originated from crosses between reconditioned males and females (wild origin fish recovered and maintained in the hatchery for >1 year after spawning) and H2 salmon originated from crosses between reconditioned males and hatchery-born females (details in Supplementary Material online). Sperm of the three groups of parents (W, H1, and H2) was used to fertilize the eggs of three wild females to create the offspring. Sperm sampling points for methylation are indicated by a red asterisk.

Fig. 2

Differentially methylated regions (DMRs). (A) DMRs found using MEDIPS showing unique and shared DMRs among groups comparisons. (B) DMRs found using Methylaction. Table: Number of DMRs detected for all possible patterns of hyper- (black squares) and hypomethylation (white squares). (**) Patterns with FDR <0.01; (*) Patterns with FDR <0.1. “Frequent” DMRs correspond to those where the methylation status of all the samples within a group is the same (3/3). Heatmap: Heatmap of normalized read count distributions for all “frequent” DMRs detected. Columns represent samples, and rows DMRs.

Fig. 3

Clustering of parents and offspring targeting those regions that were differentially methylated (DMRs) between hatchery and wild individuals in the parental group (hatchery reared fish distinctive signatures). (A) PCA using normalized total read counts of 1,000-bp sliding windows genome wide for the target regions. (B) Clustering and Heatmap of normalized read counts (log transformed) of hatchery reared fish distinctive signatures. Columns represent samples, and rows DMRs (the name of the closest/overlapping loci was assigned to each DMR).