Abstract
Epigenetic mechanisms, such as DNA methylation, can influence gene
regulation and affect phenotypic variation, raising the possibility that
they contribute to ecological adaptation. To being to address this issue
requires high-resolution sequencing studies of natural populations to
pinpoint epigenetic regions of potential ecological and evolutionary
significance. However, such studies are still relatively uncommon,
especially in insects, and are mainly restricted to a few model
organisms. Here, we characterize patterns of DNA methylation for natural
populations of Timema cristinae adapted to two host plant species (i.e.,
ecotypes). By integrating results from sequencing of whole
transcriptomes, genomes, and methylomes, we investigate whether
environmental, host, and genetic differences of these stick insects are
associated with methylation levels of cytosine nucleotides in CpG
context. We report an overall genome-wide methylation level for T.
cristinae of ~14%, being enriched in gene bodies and
impoverished in repetitive elements. Genome-wide DNA methylation
variation was strongly positively correlated with genetic distance
(relatedness), but also exhibited significant host-plant effects. Using
methylome-environment association analysis, we pinpointed specific
genomic regions that are differentially methylated between ecotypes,
with these regions being enriched for genes with functions in membrane
processes. The observed association between methylation variation with
genetic relatedness and the ecologically-important variable of host
plant suggest a potential role for epigenetic modification in T.
cristinae adaptation. To substantiate such adaptive significance, future
studies could test if methylation has a heritable component and the
extent to which it responds to experimental manipulation in field and
laboratory studies.