Data from: Resource base influences genome-wide DNA methylation levels in wild baboons (Papio cynocephalus)

Variation in resource availability commonly exerts strong effects on fitness-related traits in wild animals. However, we know little about the molecular mechanisms that mediate these effects, or about their persistence over time. To address these questions, we profiled genome-wide whole blood DNA methylation levels in two sets of wild baboons: (i) ‘wild-feeding’ baboons that foraged naturally in a savanna environment and (ii) ‘Lodge’ baboons that had ready access to spatially concentrated human food scraps, resulting in high feeding efficiency and low daily travel distances. We identified 1,014 sites (0.20% of sites tested) that were differentially methylated between wild-feeding and Lodge baboons, providing the first evidence that resource availability shapes the epigenome in a wild mammal. Differentially methylated sites tended to occur in contiguous stretches (i.e., in differentially methylated regions or DMRs), in promoters and enhancers, and near metabolism-related genes, supporting their functional importance in gene regulation. In agreement, reporter assay experiments confirmed that methylation at the largest identified DMR, located in the promoter of a key glycolysis-related gene, was sufficient to causally drive changes in gene expression. Intriguingly, all dispersing males carried a consistent epigenetic signature of their membership in a wild-feeding group, regardless of whether males dispersed into or out of this group as adults. Together, our findings support a role for DNA methylation in mediating ecological effects on phenotypic traits in the wild, and emphasize the dynamic environmental sensitivity of DNA methylation levels across the life course.

资源可获得性的差异通常会对野生动物的适合度相关性状产生显著影响。然而，目前我们对介导此类效应的分子机制，以及这些效应随时间的持续性仍知之甚少。为解答上述问题，我们对两组野生狒狒的全血全基因组DNA甲基化（DNA methylation）水平进行了谱分析：其一为在稀树草原环境中自然觅食的‘野生觅食组’狒狒；其二为可便捷获取空间聚集的人类食物残渣的‘营地组’狒狒，后者觅食效率更高且每日移动距离更短。我们共鉴定出1014个野生觅食组与营地组狒狒间的差异甲基化位点（differentially methylated sites，占检测位点的0.20%），这为资源可获得性塑造野生哺乳动物表观组（epigenome）提供了首个实证依据。差异甲基化位点多呈连续簇状分布（即形成差异甲基化区域，differentially methylated regions, DMRs），且富集于启动子与增强子区域，以及代谢相关基因附近，这印证了其在基因调控中的功能重要性。与此一致，报告基因实验（reporter assay）证实：位于关键糖酵解（glycolysis）相关基因启动子区的所鉴定出的最大DMR的甲基化水平，足以因果性地引发基因表达的改变。有趣的是，所有扩散雄性狒狒均携带与其所属野生觅食组身份一致的表观遗传特征（epigenetic signature），无论这些雄性是在成年后迁入还是迁出该群体。综上，本研究结果证实DNA甲基化在介导野外生态效应对表型性状的影响中发挥作用，并强调了DNA甲基化水平在生命全程中对环境的动态敏感性。