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

Abstract

Identifying the molecular mechanisms involved in rapid adaptation to novel environments and determining their predictability are central questions in Evolutionary Biology and pressing issues due to rapid global changes. Complementary to genetic responses to selection, faster epigenetic variations such as modifications of DNA methylation may play a substantial role in rapid adaptation. In the context of rampant urbanization, joint examinations of genomic and epigenomic mechanisms are still lacking. Here, we investigated genomic (SNP) and epigenomic (CpG methylation) responses to urban life in a passerine bird, the Great tit (Parus major). To test whether urban evolution is predictable (ie parallel) or involves mostly non-parallel molecular processes among cities, we analysed three distinct pairs of city and forest Great tit populations across Europe. Results reveal a polygenic response to urban life, with both many genes putatively under weak divergent selection and multiple differentially methylated regions (DMRs) between forest and city great tits. DMRs mainly overlapped transcription start sites and promotor regions, suggesting their importance in the modulation gene expression. Both genomic and epigenomic outliers were found in genomic regions enriched for genes with biological functions related to nervous system, immunity, behaviour, hormonal and stress responses. Interestingly, comparisons across the three pairs of city-forest populations suggested little parallelism in both genetic and epigenetic responses. Our results confirm, at both the genetic and epigenetic levels, hypotheses of polygenic and largely non-parallel mechanisms of rapid adaptation in new environments such as urbanized areas.

Ingrained city rhythms: flexible activity timing but more persistent circadian pace in urban birds

“…An important, remaining question is whether the differences in the circadian properties between city and forest birds observed here are caused by local adaptation of clocks, or are merely a phenotypic response. There is evidence that genetic change can be rapid in cities [65–67], and the phenotypic differences between city and forest birds could indeed reflect genetic differences in the response of their clocks to light. However, the high plastic nature of activity patterns and the reversible nature of clock properties (e.g.…”

An ecologist's guide for studying DNA methylation variation in wild vertebrates

“…Evolutionary ecologists now study epigenetic mechanisms to provide insights into the potential role of epigenetic variation in adaptation to changing environments. To assess the evolutionary implications, DNA methylation has been studied in relation to heritability (Hu et al, 2021;van Oers et al, 2020), whether it might be under selection (Laine et al, 2016;Skinner et al, 2014) and whether it might be involved in range expansion and adaptation (Caizergues et al, 2021;Gore et al, 2018;Heckwolf et al, 2020;Liebl et al, 2013;Meröndun et al, 2019;Riyahi et al, 2017;Schrey et al, 2012;Sheldon et al, 2018).…”

“…Hence, DNA methylation has become of great interest and, as a result, the number of studies on the causes and consequences of DNA methylation in natural populations is rising. Studies that aim to provide insights into the origin of variation in DNA methylation focus on a wide range of environmental influences, including pH (Massicotte & Angers, 2012), habitat quality (Hu et al, 2019), parasites (Hu et al, 2018; McNew et al, 2021; Wenzel & Piertney, 2014), and anthropogenic causes such as urbanization (Caizergues et al, 2021; Garcia et al, 2019; McNew et al, 2017; Riyahi et al, 2015; Watson et al, 2021) and contaminants (Laine et al, 2021; Mäkinen et al, 2021; McNew et al, 2021; Nilsen et al, 2016; Pierron et al, 2014; Romano et al, 2017). In addition, studies have now included DNA methylation changes as a possible mechanism causing phenotypic changes due to environmental experiences during early development, such as brood size (Sepers et al, 2021; Sheldon et al, 2018), diet or resource availability (Laubach et al, 2019; Lea et al, 2016; Weyrich et al, 2018), predation risk (Noguera & Velando, 2019) and parental effects (Bentz et al, 2016; Rubenstein et al, 2016; Weyrich et al, 2016).…”

Genome‐wide DNA methylation patterns harbour signatures of hatchling sex and past incubation temperature in a species with environmental sex determination

“…However, a few lines of evidence from species with genotypic sex determination support this possibility. Several studies have identified autosomal sex‐associated variation in DNAm patterns across species differing in sex‐determination system in somatic tissues (Gatev et al, 2021 ), including blood (Caizergues et al, 2021 ; Janowitz Koch et al, 2016 ), muscle (Wan et al, 2016 ) and liver (Hu et al, 2019 ; Zhuang et al, 2020 ). Some sex‐biased autosomal DNAm patterns have even been shown to be established during development and stable throughout the life course (Gatev et al, 2021 ).…”