Epigenetic variation can promote adaptation by smoothing rugged fitness landscapes

Abstract

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 is 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 without environmental change. In particular, rapid epigenetic changes can sometimes 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 those switches occur. 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 populations adaptive trajectory. Significance StatementSelection can act upon individuals with epigenetic differences, but it is unclear how much long-term effect this can have on evolutionary trajectories if the epigenetic changes only last a limited number of generations. When the environment changes or more than one functionality is needed simultaneously, it is apparent how bet hedging or division of labour can be advantageous, but what about in a single, constant environment? Here, we find that epigenetics, by allowing individuals rapid yet heritable access to multiple alternate phenotypes, can change the outcome of genetic evolution and has the tendency to remove local fitness peaks and allow adaptation to find higher optima. As such, epigenetics, despite being transient, can profoundly affect adaptive trajectories.