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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.

Genome‐wide variation in DNA methylation linked to developmental stage and chromosomal suppression of recombination in white‐throated sparrows