Does Evolutionary Plasticity Evolve?

During the development of a multicellular organism from a zygote, a large number of epigenetic interactions take place on every level of suborganismal organization. This raises the possibility that the system of epigenetic interactions may compensate or "buffer" some of the changes that occur as mutations on its lowest levels, and thus stabilize the phenotype with respect to mutations. This hypothetical phenomenon will be called "epigenetic stability." Its potential importance stems from the fact that phenotypic variation with a genetic basis is an essential prerequisite for evolution. Thus, variation in epigenetic stability might profoundly affect attainable rates of evolution. While representing a systemic property of a developmental system, epigenetic stability might itself be genetically determined and thus be subject to evolutionary change. Whether or not this is the case should ideally be answered directly, that is, by experimentation. The time scale involved and our insufficient quantitative understanding of developmental pathways will probably preclude such an approach in the foreseeable future. Preliminary answers are sought here by using a biochemically motivated model of a small but central part of a developmental pathway. Modeled are sets of transcriptional regulators that mutually regulate each other's expression and thereby form stable gene expression patterns. Such gene-expression patterns, crucially involved in determining developmental pattern formation events, are most likely subject to strong stabilizing natural selection. After long periods of stabilizing selection, the fraction of mutations causing changes in gene-expression patterns is substantially reduced in the model. Epigenetic stability has increased. This phenomenon is found for widely varying regulatory scenarios among transcription factor genes. It is discussed that only epistatic (nonlinear) gene interactions can cause such change in epigenetic stability. Evidence from paleontology, molecular evolution, development, and genetics, consistent with the existence of variation in epigenetic stability, is discussed. The relation of epigenetic stability to developmental canalization is outlined. Experimental scenarios are suggested that may provide further evidence.