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 non-parallel 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 non-parallel mechanisms of
rapid adaptation in novel environments such as urbanized areas.