Epigenetic inheritance systems act as a bridge between ecological and evolutionary timescales

Abstract

A long-standing problem in biology is reconciling phenotypic change and stability. Organisms are extraordinarily plastic, responding to life-stage transitions, seasonal cues, and environmental change. Some of these changes are permanent and some are reversible occurring thousands of times during a lifetime. Yet, at the same time, phenotypic stability is equally evident, enabling reliable assignment of individuals into morphs, populations, and species. A key question in evolution is how these timescales of phenotypic change are linked. The traditional view is that they are not such that there is a dichotomy of “ephemeral environmental effects” and “stable genetic effects” with only the latter relevant to evolutionary change. However, as Ledon-Rettig et al.’s review shows, this view needs to be updated as we learn more about the proximate mechanisms behind genetic and epigenetic determinants of phenotypic variation. Purely environmental influences on the phenotype are often assumed to be more transient than genetic effects and thus not important for long-term evolutionary change. However, environmental influences on the phenotype are often more stable then genetic influences—the most extreme example being the influence of gravitational forces—a factor that has consistently influenced the form and function of all organisms. However, genetic influences on the phenotype are often assumed to be the most stable. Yet, genetic variants that map onto phenotypic variation consistently irrespective of the environmental and genetic context are extremely rare. Instead, the phenotypic effects of specific DNA sequences is often highly variable from one generation to the next depending on both genetic background and environmental context. Similarly, as Ledon-Rettig et al. show, the stability of epigenetic effects are also not easily categorized and can range from transitory cell state modifications that can change over the course of development to multigenerational influences of a mother’s behavior on her descendants. These observations show that there is not a simple dichotomy in the timescales of phenotypic expression and that a more realistic view is of a gradation of stability that does not map onto genes versus environment in a simple way.