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

ABSTRACT: 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.

SUBMITTER: Sun D

PROVIDER: S-EPMC8359194 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background Earlier breeding is one of the strongest responses to global change in birds and is a key factor determining reproductive success. In most studies of climate effects, the focus has been on large-scale environmental indices or temperature averaged over large geographical areas, neglecting that animals are affected by the local conditions in their home ranges. In riverine ecosystems, climate change is altering the flow regime, in addition to changes resulting from the increasing demand for renewable and clean hydropower. Together with increasing temperatures, this can lead to shifts in the time window available for successful breeding of birds associated with the riverine habitat. Here, we investigated specifically how the environmental conditions at the territory level influence timing of breeding in a passerine bird with an aquatic lifestyle, the white-throated dipper Cinclus cinclus. We relate daily river discharge and other important hydrological parameters, to a long-term dataset of breeding phenology (1978–2015) in a natural river system. Results Dippers bred earlier when winter river discharge and groundwater levels in the weeks prior to breeding were high, and when there was little snow in the catchment area. Breeding was also earlier at lower altitudes, although the effect dramatically declined over the period. This suggests that territories at higher altitudes had more open water in winter later in the study period, which permitted early breeding also here. Unexpectedly, the largest effect inducing earlier breeding time was territory river discharge during the winter months and not immediately prior to breeding. The territory river discharge also increased during the study period. Conclusions The observed earlier breeding can thus be interpreted as a response to climate change. Measuring environmental variation at the scale of the territory thus provides detailed information about the interactions between organisms and the abiotic environment.

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

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