Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA, USA.
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, USA.
Genome Biol Evol. 2024 Feb 1;16(2). doi: 10.1093/gbe/evae022.
There is great interest in exploring epigenetic modifications as drivers of adaptive organismal responses to environmental change. Extending this hypothesis to populations, epigenetically driven plasticity could influence phenotypic changes across environments. The canonical model posits that epigenetic modifications alter gene regulation and subsequently impact phenotypes. We first discuss origins of epigenetic variation in nature, which may arise from genetic variation, spontaneous epimutations, epigenetic drift, or variation in epigenetic capacitors. We then review and synthesize literature addressing three facets of the aforementioned model: (i) causal effects of epigenetic modifications on phenotypic plasticity at the organismal level, (ii) divergence of epigenetic patterns in natural populations distributed across environmental gradients, and (iii) the relationship between environmentally induced epigenetic changes and gene expression at the molecular level. We focus on DNA methylation, the most extensively studied epigenetic modification. We find support for environmentally associated epigenetic structure in populations and selection on stable epigenetic variants, and that inhibition of epigenetic enzymes frequently bears causal effects on plasticity. However, there are pervasive confounding issues in the literature. Effects of chromatin-modifying enzymes on phenotype may be independent of epigenetic marks, alternatively resulting from functions and protein interactions extrinsic of epigenetics. Associations between environmentally induced changes in DNA methylation and expression are strong in plants and mammals but notably absent in invertebrates and nonmammalian vertebrates. Given these challenges, we describe emerging approaches to better investigate how epigenetic modifications affect gene regulation, phenotypic plasticity, and divergence among populations.
人们对于探索表观遗传修饰作为生物体对环境变化的适应性反应的驱动因素非常感兴趣。将这一假设扩展到种群中，表观遗传驱动的可塑性可以影响跨环境的表型变化。经典模型假设，表观遗传修饰改变基因调控，进而影响表型。我们首先讨论了自然界中表观遗传变异的起源，这些变异可能来自遗传变异、自发的表观突变、表观遗传漂变或表观遗传调节剂的变异。然后，我们回顾并综合了文献，讨论了上述模型的三个方面：（i）表观遗传修饰对生物体水平上表型可塑性的因果影响，（ii）在环境梯度分布的自然种群中表观遗传模式的分歧，以及（iii）环境诱导的表观遗传变化与分子水平上基因表达之间的关系。我们专注于 DNA 甲基化，这是研究最多的表观遗传修饰。我们发现支持在种群中存在与环境相关的表观遗传结构和对稳定表观遗传变异的选择，并且抑制表观遗传酶通常对可塑性具有因果影响。然而，文献中存在普遍的混杂问题。染色质修饰酶对表型的影响可能独立于表观遗传标记，或者是由于与表观遗传学无关的功能和蛋白质相互作用所致。在植物和哺乳动物中，环境诱导的 DNA 甲基化变化与表达之间的关联非常强，但在无脊椎动物和非哺乳动物脊椎动物中明显不存在。鉴于这些挑战，我们描述了一些新兴的方法，可以更好地研究表观遗传修饰如何影响基因调控、表型可塑性以及种群间的分歧。
