Pappas Fotis, Johnsson Martin, Andersson Göran, Debes Paul V, Palaiokostas Christos
Department of Animal Biosciences, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Department of Aquaculture and Fish Biology, Hólar University, Sauðárkrókur, Iceland.
Heredity (Edinb). 2025 May;134(5):293-305. doi: 10.1038/s41437-025-00756-y. Epub 2025 Mar 18.
Differential DNA methylation due to epigenetic phenomena is crucial in regulating gene expression. Understanding the consequences of such differential expression on sperm quality parameters may provide insights into the underlying mechanisms of male reproductive success. Nonetheless, male fertility in fish remains understudied despite its critical importance to overall reproductive success in nature and captivity. This study investigated the DNA methylation landscape in spermatozoa of domesticated Arctic charr (Salvelinus alpinus) and its associations with sperm quality parameters. Computer assisted-semen analysis (CASA) was performed in 47 sperm samples of farmed Arctic charr, followed by enzymatic methylation sequencing (EM-seq). Our results showed that the DNA of Arctic charr sperm is highly methylated (mean value of ~86%), though variations were observed in genomic features involved in gene regulation. Methylation at variable CpG sites exhibited regional correlation decaying by physical distance, while methylation similarities among individuals were strongly coupled with genetic variation and mirrored pedigree structure. Comethylation network analyses for promoters, CpG islands and first introns revealed genomic modules significantly correlated with sperm quality traits (p < 0.05; Bonferroni adjusted), with distinct patterns suggesting a resource trade-off between sperm concentration and kinematics. Furthermore, annotation and gene-set enrichment analysis highlighted biological mechanisms related to spermatogenesis, cytoskeletal regulation, and mitochondrial function, all vital to sperm physiology. These findings suggest that DNA methylation is a critical and fundamental factor influencing male fertility in Arctic charr, providing insights into the underlying mechanisms of male reproductive success.
由于表观遗传现象导致的DNA甲基化差异在调节基因表达中至关重要。了解这种差异表达对精子质量参数的影响可能有助于深入了解雄性生殖成功的潜在机制。尽管如此，鱼类的雄性生育力尽管对自然和圈养环境中的整体繁殖成功至关重要，但仍未得到充分研究。本研究调查了养殖北极红点鲑（Salvelinus alpinus）精子中的DNA甲基化图谱及其与精子质量参数的关联。对47个养殖北极红点鲑的精子样本进行了计算机辅助精液分析（CASA），随后进行了酶促甲基化测序（EM-seq）。我们的结果表明，北极红点鲑精子的DNA高度甲基化（平均值约为86%），尽管在参与基因调控的基因组特征中观察到了差异。可变CpG位点的甲基化表现出区域相关性随物理距离衰减，而个体之间的甲基化相似性与遗传变异密切相关，并反映了谱系结构。对启动子、CpG岛和第一个内含子的共甲基化网络分析揭示了与精子质量性状显著相关的基因组模块（p < 0.05；经Bonferroni校正），不同的模式表明精子浓度和运动学之间存在资源权衡。此外，注释和基因集富集分析突出了与精子发生、细胞骨架调节和线粒体功能相关的生物学机制，所有这些对精子生理学都至关重要。这些发现表明，DNA甲基化是影响北极红点鲑雄性生育力的关键和基本因素，为雄性生殖成功的潜在机制提供了见解。
