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