Unveiling the epigenetic signatures: DNA methylation patterns in the social hierarchies of male giant freshwater prawns (Macrobrachium rosenbergii)

IF 3.9 1区农林科学 Q1 FISHERIES

Aquaculture Pub Date : 2025-06-13 DOI:10.1016/j.aquaculture.2025.742838

Liping Li , Jiongying Yu , Zhenglong Xia , Quanxin Gao , Qiongying Tang , Shaokui Yi

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引用次数: 0

Abstract

DNA methylation is a cornerstone of epigenetic regulation, yet its role in shaping social hierarchies within crustacean species remains poorly characterized. This study investigated the giant freshwater prawn (Macrobrachium rosenbergii, GFP), which exhibits distinct male morphotypes (blue claws [BC], orange claws [OC], and small males [SM]) and offers a compelling model for studying epigenetic regulation of phenotypic plasticity. Our population analysis revealed a morphotype distribution of 21.37 % BC, 63.36 % OC, and 15.27 % SM. Through comprehensive whole-genome bisulfite sequencing (WGBS) analysis, we identified 211 differentially methylated regions (DMRs) across morphotype comparisons (BC vs. OC, BC vs. SM, OC vs. SM), comprising 77 hypermethylated and 136 hypomethylated regions. These DMRs were functionally associated with 150 differentially methylated genes (DMGs), including 60 hypermethylated and 99 hypomethylated. Notably, hypomethylation of the vg (vitellogenin) 5′ untranslated region in OC individuals enhanced reproductive responsiveness. Additionally, the hypomethylated DMG hspg2 (heparan sulfate proteoglycan 2) exhibited significant upregulation in BC group, potentially conferring a selective advantage in limb regeneration—thereby reinforcing social dominance behaviors. Moreover, hypomethylation and concurrent upregulation of the mitochondrial idh2 ([NADP]-dependent isocitrate dehydrogenase 2) in SM individuals may underpin a specialized reproductive strategy by optimizing energy metabolism. This study provides insights into the intricate interplay between epigenetic modifications—particularly DNA methylation—and male GFP morphotype diversification. These findings also advance our understanding of epigenetic contributions to phenotypic variation in non-model arthropods and establish a foundation for future research on transgenerational epigenetics in aquatic species.

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揭示表观遗传特征：雄性罗氏沼虾（Macrobrachium rosenbergii）社会等级中的DNA甲基化模式

DNA甲基化是表观遗传调控的基石，但其在甲壳类动物物种中形成社会等级的作用仍不清楚。本研究以罗氏沼虾（Macrobrachium rosenbergii， GFP）为研究对象，该虾具有不同的雄性形态（蓝爪[BC]、橙爪[OC]和小雄虾[SM]），为研究表型可塑性的表观遗传调控提供了一个令人信服的模型。种群分析显示BC占21.37%，OC占63.36%，SM占15.27%。通过全面的全基因组亚硫酸氢盐测序（WGBS）分析，我们在形态比较（BC与OC、BC与SM、OC与SM）中确定了211个差异甲基化区域（DMRs），包括77个高甲基化区域和136个低甲基化区域。这些DMRs在功能上与150个差异甲基化基因（dmg）相关，包括60个高甲基化基因和99个低甲基化基因。值得注意的是，OC个体卵黄原蛋白5 '非翻译区的低甲基化增强了生殖反应性。此外，低甲基化的DMG hspg2（硫酸肝素蛋白多糖2）在BC组中表现出显著的上调，可能在肢体再生中具有选择性优势，从而加强了社会优势行为。此外，SM个体的低甲基化和线粒体idh2 （[NADP]依赖性异柠檬酸脱氢酶2）的同步上调可能通过优化能量代谢来支持特殊的生殖策略。这项研究为表观遗传修饰（尤其是DNA甲基化）和雄性绿色荧光蛋白形态多样化之间复杂的相互作用提供了见解。这些发现也促进了我们对非模式节肢动物表型变异的表观遗传学贡献的理解，并为未来水生物种跨代表观遗传学的研究奠定了基础。

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来源期刊

Aquaculture 农林科学-海洋与淡水生物学

CiteScore

8.60

自引率

17.80%

发文量

1246

审稿时长

56 days

期刊介绍： Aquaculture is an international journal for the exploration, improvement and management of all freshwater and marine food resources. It publishes novel and innovative research of world-wide interest on farming of aquatic organisms, which includes finfish, mollusks, crustaceans and aquatic plants for human consumption. Research on ornamentals is not a focus of the Journal. Aquaculture only publishes papers with a clear relevance to improving aquaculture practices or a potential application.