Pereira Paulo, Afonso Sandra, Múrias António, Carneiro Miguel, Sabatino Stephen J
CIBIO - Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Vairão, Portugal.
BIOPOLIS - Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal.
J Mol Evol. 2025 Jun 2. doi: 10.1007/s00239-025-10253-9.
Epigenetic modifications are one of the evolutionary mechanisms that allow individuals and populations to adapt to environmental changes. However, the relative importance of epigenetic versus genetic changes in adaptation and how they may interact remains poorly understood. Here, we investigate the role of DNA methylation in adaptation by studying a population of Allis shad (Alosa alosa) that evolved a completely freshwater life history approximately 70 years ago and the anadromous one that founded it. Using reduced representation bisulfite sequencing, we identified 227 differentially methylated regions (DMRs) between them, overlapping known important genes for freshwater adaptation, such as ATP2B4, PRLH2, and KCNF1A. Enrichment analysis of GO terms suggested that genes in the identified DMRs play key roles in neural, growth, and developmental functions, which is concordant with previous studies on adaptation to freshwater in this species and genus. Using pool-seq data from an earlier study, we then tested if the DMRs for freshwater shad found here overlapped genomic outlier regions that may be under genetic selection in three independently evolved, freshwater populations (including the one studied here). Our analysis showed that the DMRs identified here fall broadly outside genomic regions under natural selection. However, 45% of these were associated with CpG > TpG deamination events in DMRs, a mutation tightly linked with DNA methylation. Our study illustrates that both genetic and epigenetic mechanisms are important during the initial stages of adaptation in this system. It also supports the hypothesis that methylation may generate polymorphism that fuels adaptive evolution.
表观遗传修饰是使个体和种群能够适应环境变化的进化机制之一。然而，表观遗传变化与遗传变化在适应过程中的相对重要性以及它们如何相互作用，仍知之甚少。在这里，我们通过研究一群美洲西鲱（Alosa alosa）来探究DNA甲基化在适应过程中的作用，这群美洲西鲱大约在70年前进化出了完全淡水生活史，其溯河洄游型祖先则构成了它们的基础。通过简化代表性亚硫酸氢盐测序，我们在它们之间鉴定出227个差异甲基化区域（DMRs），这些区域与已知的淡水适应重要基因重叠，如ATP2B4、PRLH2和KCNF1A。基因本体（GO）术语富集分析表明，鉴定出的DMRs中的基因在神经、生长和发育功能中起关键作用，这与之前关于该物种和属适应淡水的研究一致。然后，我们利用早期研究中的群体测序数据，测试这里发现的淡水西鲱的DMRs是否与三个独立进化的淡水种群（包括这里研究的种群）中可能处于遗传选择下的基因组异常区域重叠。我们的分析表明，这里鉴定出的DMRs大致落在自然选择下的基因组区域之外。然而，其中45%与DMRs中的CpG>TpG脱氨基事件相关，这种突变与DNA甲基化紧密相连。我们的研究表明，在这个系统的适应初始阶段，遗传和表观遗传机制都很重要。它还支持了甲基化可能产生多态性从而推动适应性进化的假设。
