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 nonpara