Data from: Fine-scale population epigenetic structure in relation to gastro-intestinal parasite load in red grouse (Lagopus lagopus scotica)

Epigenetic modification of cytosine methylation states can be elicited by environmental stresses and may be a key process affecting phenotypic plasticity and adaptation. Parasites are potent stressors with profound physiological and ecological effects on their host, but there is little understanding in how parasites may influence host methylation states. Here, we estimate epigenetic diversity and differentiation among 21 populations of red grouse (Lagopus lagopus scotica) in north-east Scotland, and test for association of gastro-intestinal parasite load (caecal nematode Trichostrongylus tenuis) with hepatic genome-wide and locus-specific methylation states. Following methylation-sensitive AFLP (MSAP), 129 bands, representing 73 methylation-susceptible and 56 non-methylated epiloci, were scored across 234 individuals. The populations differed significantly in genome-wide methylation levels and were also significantly epigenetically (FST = 0.0227; p < 0.001) and genetically (FST = 0.0058; p < 0.001) differentiated. Parasite load was not associated with either genome-wide methylation levels or epigenetic differentiation. Instead, we found eight disproportionately differentiated epilocus-specific methylation states (FST -outliers) using bayescan software and significant positive and negative association of 35 methylation states with parasite load from bespoke generalised estimating equations (GEE), simple logistic regression (sam) and Bayesian environmental analysis (bayenv). Following Sanger sequencing, genome mapping and geneontology (go) annotation, some of these epiloci were linked to genes involved in regulation of cell cycle, signalling, metabolism, immune system and notably rRNA methylation, histone acetylation and small RNAs. These findings demonstrate an epigenetic signature of parasite load in populations of a wild bird and suggest intriguing physiological effects of parasite-associated cytosine methylation.

胞嘧啶甲基化状态的表观遗传修饰可由环境胁迫诱导，或许是影响表型可塑性与适应性的关键过程。寄生虫作为强效胁迫因子，对宿主具有深远的生理与生态效应，但目前对寄生虫如何影响宿主甲基化状态的认知仍较为匮乏。本研究对苏格兰东北部21个红松鸡（Lagopus lagopus scotica）种群的表观遗传多样性与分化程度进行评估，并检验胃肠道寄生虫负荷（盲肠线虫Trichostrongylus tenuis）与肝脏全基因组及位点特异性甲基化状态的关联。在采用甲基化敏感扩增多态性（methylation-sensitive AFLP, MSAP）技术后，我们在234个个体中共分型得到129个条带，其中包含73个易受甲基化影响的表观位点与56个非甲基化表观位点。种群间的全基因组甲基化水平存在显著差异，同时在表观遗传层面（FST=0.0227; p<0.001）与遗传层面（FST=0.0058; p<0.001）均呈现显著分化。寄生虫负荷与全基因组甲基化水平及表观遗传分化均无关联。与之相反，我们通过Bayescan软件鉴定出8个分化程度异常的位点特异性甲基化状态（FST离群位点），并通过定制化广义估计方程（GEE）、简单逻辑回归（sam）及贝叶斯环境分析（bayenv）发现35个甲基化状态与寄生虫负荷存在显著的正负相关关系。经桑格测序、基因组定位及基因本体论（GO）注释后，我们发现部分表观位点与参与细胞周期调控、信号通路、代谢、免疫系统调控的基因相关，尤其涉及核糖体RNA甲基化、组蛋白乙酰化及小RNA相关通路。本研究结果证实野生鸟类种群中存在与寄生虫负荷相关的表观遗传特征，并提示寄生虫关联的胞嘧啶甲基化具有潜在的重要生理效应。