Epigenetic variation can promote adaptation by smoothing rugged fitness landscapes

Heritable non-genetic phenotypic variation-broadly, epigenetics can
potentially influence evolutionary outcomes as direct targets of selection
or through interactions with genetic variation. While their evolutionary
benefits in generating phenotypic diversity in changing environments are
well-characterized, there has been relatively little consideration of how
the joint influence of epigenetic changes and mutations would affect
traversal of multi-peak adaptive landscapes. Here, we discover general
principles for how epigenetics, by generating an epigenetic quasispecies
(clusters of semi-stable phenotypes mapped to a single genotype), tends to
improve adaptive outcomes of an asexual population on rugged fitness
landscapes even in a constant environment. In particular, rapid epigenetic
changes tend to smooth out suboptimal fitness peaks through incorporating
fitness contributions of epimutations, allowing access to better adaptive
outcomes. Remarkably, the average impact of epigenetics is more strongly
influenced by an approximate balance between switching rates rather than
the absolute rate at which switching occurs. These findings demonstrate
that epigenetic changes can be influential even without having strong
heritability and have a striking, yet generally invisible, beneficial role
in shaping a population's adaptive trajectory.