School of Biological Sciences, University of Aberdeen, Aberdeen, Scotland.
Centre for Evolutionary Hologenomics, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
Insect Mol Biol. 2024 Oct;33(5):516-533. doi: 10.1111/imb.12933. Epub 2024 Jun 12.
Many species are threatened by climate change and must rapidly respond to survive in changing environments. Epigenetic modifications, such as DNA methylation, can facilitate plastic responses by regulating gene expression in response to environmental cues. Understanding epigenetic responses is therefore essential for predicting species' ability to rapidly adapt in the context of global environmental change. Here, we investigated the functional significance of different methylation-associated cellular processes on temperature-dependent life history in seed beetles, Callosobruchus maculatus Fabricius 1775 (Coleoptera: Bruchidae). We assessed changes under thermal stress in (1) DNA methyltransferase (Dnmt1 and Dnmt2) expression levels, (2) genome-wide methylation and (3) reproductive performance, with (2) and (3) following treatment with 3-aminobenzamide (3AB) and zebularine (Zeb) over two generations. These drugs are well-documented to alter DNA methylation across the tree of life. We found that Dnmt1 and Dnmt2 were expressed throughout the body in males and females, but were highly expressed in females compared with males and exhibited temperature dependence. However, whole-genome methylation did not significantly vary with temperature, and only marginally or inconclusively with drug treatment. Both 3AB and Zeb led to profound temperature-dependent shifts in female reproductive life history trade-off allocation, often increasing fitness compared with control beetles. Mismatch between magnitude of treatment effects on DNA methylation versus life history effects suggest potential of 3AB and Zeb to alter reproductive trade-offs via changes in DNA repair and recycling processes, rather than or in addition to (subtle) changes in DNA methylation. Together, our results suggest that epigenetic mechanisms relating to Dnmt expression, DNA repair and recycling pathways, and possibly DNA methylation, are strongly implicated in modulating insect life history trade-offs in response to temperature change.
许多物种受到气候变化的威胁，必须迅速响应才能在不断变化的环境中生存。表观遗传修饰，如 DNA 甲基化，可以通过调节基因表达来响应环境线索，从而促进可塑性反应。因此，了解表观遗传反应对于预测物种在全球环境变化背景下快速适应的能力至关重要。在这里，我们研究了不同甲基化相关细胞过程在温度依赖性种子象鼻虫（Callosobruchus maculatus Fabricius 1775）（鞘翅目：象甲科）生活史中的功能意义。我们评估了在热应激下（1）DNA 甲基转移酶（Dnmt1 和 Dnmt2）表达水平、（2）全基因组甲基化和（3）生殖性能的变化，其中（2）和（3）在两代中用 3-氨基苯甲酰胺（3AB）和 zebularine（Zeb）处理。这些药物在整个生命树中都被很好地记录下来，可以改变 DNA 甲基化。我们发现，Dnmt1 和 Dnmt2 在雄性和雌性的整个身体中都有表达，但在雌性中的表达水平远高于雄性，并表现出温度依赖性。然而，全基因组甲基化与温度没有显著变化，与药物处理也只有轻微或不确定的变化。3AB 和 Zeb 都导致了雌性生殖生活史权衡分配的显著的温度依赖性变化，通常与对照甲虫相比增加了适应性。处理对 DNA 甲基化的影响与对生活史的影响之间的不匹配表明，3AB 和 Zeb 有可能通过改变 DNA 修复和回收过程来改变生殖权衡，而不仅仅是（微妙的）改变 DNA 甲基化。总之，我们的结果表明，与 Dnmt 表达、DNA 修复和回收途径相关的表观遗传机制，以及可能的 DNA 甲基化，强烈暗示它们在调节昆虫生活史权衡以应对温度变化方面发挥作用。
