Urbanization is associated with modifications in DNA methylation in a small passerine bird

Abstract

Urbanization represents a fierce driver of phenotypic change, yet the molecular mechanisms underlying observed phenotypic patterns are poorly understood. Epigenetic changes are expected to facilitate more rapid adaption to changing or novel environments, such as our towns and cities, compared with slow changes in gene sequence. A comparison of liver and blood tissue from great tits Parus major originating from an urban and a forest site demonstrated that urbanization is associated with variation in genome‐wide patterns of DNA methylation. Combining reduced representation bisulphite sequencing with transcriptome data, we revealed habitat differences in DNA methylation patterns that suggest a regulated and coordinated response to the urban environment. In the liver, genomic sites that were differentially methylated between urban‐ and forest‐dwelling birds were over‐represented in regulatory regions of the genome and more likely to occur in expressed genes. DNA methylation levels were also inversely correlated with gene expression at transcription start sites. Furthermore, differentially methylated CpG sites, in liver, were over‐represented in pathways involved in (i) steroid biosynthesis, (ii) superoxide metabolism, (iii) secondary alcohol metabolism, (iv) chylomicron remodelling, (v) cholesterol transport, (vi) reactive oxygen species (ROS) metabolic process and (vii) epithelial cell proliferation. This corresponds with earlier studies identifying diet and exposure to ROS as two of the main drivers of divergence between organisms in urban and nonurban environments. Conversely, in blood, sites that were differentially methylated between urban‐ and forest‐dwelling birds were under‐represented in regulatory regions, more likely to occur in nonexpressed genes and not over‐represented in specific biological pathways. It remains to be determined whether diverging patterns of DNA methylation represent adaptive evolutionary responses and whether the conclusions can be more widely attributed to urbanization.

Testing for parallel genomic and epigenomic footprints of adaptation to urban life in a passerine bird

“…Contrary to the common prediction that living in cities is likely to influence epigenomes (24, 25), no genome wide pattern of differentiation in methylation between urban and forest great tits was detected. However, we observed a difference in mean methylation level between birds from Warsaw and Barcelona on their autosomes, as well as between males and females on the Z chromosome, showing that methylation differences were identifiable.…”

“…In line with these results, GO analyses revealed enrichment in genes associated with neuronal functions, behaviour, but also blood, immune and endocrine systems (Table S9, Figure S3), revealing the potential need of physiological adjustments in urban habitats. Surprisingly, a recent study on great tit differences of methylation between city and forest habitats in another European city found no GO enrichment in blood, while some in liver tissue (Watson et al 2020, note that they investigated DMSs, Differentially Methylated Sites, which differs from DMRs identified here). These contrasted results highlight the fact that methylation patterns highly depend on the analysed tissues (11), and show, once more, that urban linked methylation might not be similar from one city to another.…”

“…CC-BY-NC-ND 4.0 International license perpetuity. It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted February 10, 2021. ; https://doi.org/10.1101/2021.02.10.430452 doi: bioRxiv preprint Contrary to the common prediction that living in cities is likely to influence epigenomes (24,25), no genome wide pattern of differentiation in methylation between urban and forest great tits was detected. However, we observed a difference in mean methylation level between birds from Warsaw and Barcelona on their autosomes, as well as between males and females on the Z chromosome, showing that methylation differences were identifiable.…”

“…It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted February 10, 2021. ; https://doi.org/10.1101/2021.02.10.430452 doi: bioRxiv preprint to be greater in urban areas than in any other habitat types, including non-urban anthropogenic contexts (18,19). The exploration of the molecular mechanisms implicated in urban-driven phenotypic changes has only begun, with both genetic (20)(21)(22), and epigenetic investigations (23)(24)(25). For instance, DNA methylation variations have been associated in vertebrates with high levels of traffic-related air pollution (e.g.…”

Urban evolution comes into its own: Emerging themes and future directions of a burgeoning field

“…Although urbanization negatively influences the survival of great tits, there appears to be the potential for adaptive evolution in fledgling traits. Specifically, Watson (2020) identified putatively adaptive epigenetic markers in blood and liver tissue of fledgling great tits. DNA methylation sites in the liver were enriched within regulatory regions, suggesting that there is gene expression variation in metabolic processes between urban and forest birds that may increase fitness.…”