Much of our knowledge on regulatory impacts of DNA methylation has come from laboratory-bred model organisms, which may not exhibit the full extent of variation found in wild populations. Here, we investigated naturally-occurring variation in DNA methylation in a wild avian species, the white-throated sparrow (Zonotrichia albicollis). This species offers exceptional opportunities for studying the link between genetic differentiation and phenotypic traits because of a nonrecombining chromosome pair linked to both plumage and behavioural phenotypes. Using novel single-nucleotide resolution methylation maps and gene expression data, we show that DNA methylation and the expression of DNA methyltransferases are significantly higher in adults than in nestlings. Genes for which DNA methylation varied between nestlings and adults were implicated in development and cell differentiation and were located throughout the genome. In contrast, differential methylation between plumage morphs was concentrated in the nonrecombining chromosome pair. Interestingly, a large number of CpGs on the nonrecombining chromosome, localized to transposable elements, have undergone dramatic loss of DNA methylation since the split of the ZAL2 and ZAL2^m chromosomes. Changes in methylation predicted changes in gene expression for both chromosomes. In summary, we demonstrate changes in genome-wide DNA methylation that are associated with development and with specific functional categories of genes in white-throated sparrows. Moreover, we observe substantial DNA methylation reprogramming associated with the suppression of recombination, with implications for genome integrity and gene expression divergence. These results offer an unprecedented view of ongoing epigenetic reprogramming in a wild population.

中文翻译：

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DNA甲基化的全基因组变异与白喉麻雀的发育阶段和染色体抑制重组有关

我们关于 DNA 甲基化调控影响的大部分知识都来自实验室培育的模式生物，它们可能不会表现出在野生种群中发现的全部变异程度。在这里，我们研究了野生鸟类物种白喉麻雀（Zonotrichia albicollis）中 DNA 甲基化的自然发生变异。）。由于与羽毛和行为表型相关的非重组染色体对，该物种为研究遗传分化和表型特征之间的联系提供了特殊的机会。使用新的单核苷酸分辨率甲基化图谱和基因表达数据，我们表明成虫的 DNA 甲基化和 DNA 甲基转移酶的表达明显高于雏鸟。DNA甲基化在雏鸟和成鸟之间变化的基因与发育和细胞分化有关，并且位于整个基因组中。相比之下，羽毛形态之间的差异甲基化集中在非重组染色体对中。有趣的是，非重组染色体上的大量 CpG，定位于转座元件，^m条染色体。甲基化的变化预测了两条染色体基因表达的变化。总之，我们证明了全基因组 DNA 甲基化的变化，这些变化与白喉麻雀的发育和基因的特定功能类别相关。此外，我们观察到与重组抑制相关的大量 DNA 甲基化重编程，对基因组完整性和基因表达差异有影响。这些结果为野生种群中正在进行的表观遗传重编程提供了前所未有的视角。