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

Abstract

DNA methylation is known to play critical roles in key biological processes. Most 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 non-recombining chromosome pair linked to both plumage and behavioral 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 localized to the non-recombining chromosome pair. One subset of CpGs on the non-recombining chromosome was extremely hypomethylated and localized to transposable elements. 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.

Sparrows and supergenes: Ecological epigenetics in action

“…Intriguingly, however, CpG sites that are extremely hypomethylated on ZAL2 m are depleted for ZAL2 m ‐specific ATAC‐seq peaks, suggesting that other regulatory mechanisms compensate to keep chromatin closed around these TE‐dense, hypomethylated regions. Thus, while common assumptions about how DNA methylation relates to function are broadly upheld by this data set, Sun et al (2021) illustrate the substantial variation that complicates these rule‐of‐thumb patterns.…”

“…In this issue of Molecular Ecology , Sun et al, (2021) address this gap by investigating divergence and diversity in DNA methylation levels in white‐throated sparrows ( Zonotrichia albicollis ), a species that segregates for two naturally occurring morphs: a more aggressive white‐striped morph and a less aggressive tan‐striped morph (Figure 1; Lowther 1961; Horton et al, 2014, Sun et al, 2018). Both of these phenotypes are linked to an ~100‐Mb rearrangement on the ZAL2 chromosome (ZAL2 m ), such that white‐striped sparrows are heterozygous for the rearrangement (ZAL2/ZAL2 m ), while tan‐striped morphs are homozygous for the standard chromosomal arrangement (ZAL2/ZAL2; Sun et al 2018).…”

“…Follow‐up studies that establish the causal or mediating role of DNA methylation levels in this fascinating genotype–phenotype relationship would be an exciting next step for this system, and for ecological epigenetics more broadly. Already, though, Sun et al (2021) demonstrate the increasing feasibility of using ecological epigenetic approaches to understand evolutionary change in natural populations of nonmodel species.…”

Supergenes on Steroids

“…Second, in both species, homozygous inversion carriers are rare (white-throated sparrows) or absent (ruffs) meaning that for the inversion haplotypes, recombination is severely hindered. Third, for genes with clear differences in sequence, allelic imbalance in gene expression seems to be a common feature of genes inside these inversions [57,73,74]. Here, we have taken a close look at the genes inside each of these inversion polymorphisms to determine what other commonalities may exist at the genetic level.…”

A supergene-linked estrogen receptor drives alternative phenotypes in a polymorphic songbird

“…Amplicons were pooled per sample, indexed, and then pooled for a single sequencing run (PE300) on an Illumina MiSeq system. Reads were filtered, trimmed, and aligned to a bisulfite-converted, N-masked reference genome, and then assigned to an allele (65). Allele-specific methylation was determined by Bismark (66).…”