Epigenetics and the city: Non-parallel DNA methylation modifications across pairs of urban-forest Great tit populations.

Aude E Caizergues,Jeremy Le Luyer,Juan-Carlos Senar,Arnaud Grégoire,Anne Charmantier,Marta Szulkin,Charles Perrier

doi:10.1111/eva.13334

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 (i.e. parallel) or involves mostly nonparallel molecular processes among cities, we analysed both SNP and CpG methylation variations across three distinct pairs of city and forest Great tit populations in Europe. Our analyses 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 modulating gene expression. Both genomic and epigenomic outliers were found in genomic regions enriched for genes with biological functions related to the nervous system, immunity, or behavioural, 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 nonparallel mechanisms of rapid adaptation in novel environments such as urbanized areas.

Highlights

Identifying mechanisms involved in rapid adaptation to novel environmental conditions is a central theme in evolutionary biology and a pressing concern in the context of global changes characterising the Anthropocene (Malhi, 2017)
This study uses genomic and epigenomic analyses to decipher the potential molecular bases implicated in phenotypic shifts and adaptation in several urban populations of a passerine bird, the Great tit
While we found weak average differentiation of the methylome between urban and forest birds, suggesting an absence of genome-wide epigenetic deregulations, we identified several differentially methylated regions between urban and forest birds, mostly non-repeated between pairs

Summary

Introduction

Identifying mechanisms involved in rapid adaptation to novel environmental conditions is a central theme in evolutionary biology and a pressing concern in the context of global changes characterising the Anthropocene (Malhi, 2017). The vast majority of studies investigating mechanisms involved in rapid adaptation to new environments have focused on phenotypic plasticity on the one hand and on genetic responses to selection on the other hand. Environmental variations can induce differences in DNA methylation patterns and modulate gene expression and upper-level phenotypes (Duncan et al, 2014; Jaenisch & Bird, 2003). Such methylation-linked phenotypic variation can occur during an individual’s lifetime, especially early on during the organism’s development (Waterland & Jirtle, 2003; Weaver et al, 2004). There is an urgent need for further empirical investigations of simultaneously rapid genetic and epigenetic evolution in response to environmental change (Danchin et al, 2011)

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Results

Conclusion