From epigenetic landscape to genetic assimilation: Revisiting Waddington's experiments

Seventy years ago, Waddington performed a series of experiments demonstrating the phenomenon of "genetic assimilation", a process by which an environmentally induced phenotype becomes stably inherited without the stimulus after not many generations of selection. While the concept has attracted much debate since then, there have been few experiments to quantitatively characterize the phenomenon. Today, we revisit Waddington's original experiments and follow-up studies that attempted to replicate his results. We summarize those experimental results in four curves: the increasing penetrance of the new phenotype, the stable frequency of unviable individuals, the delayed appearance of assimilated individuals, and the quick fixation of the assimilated lineage. We then present a theoretical model to illustrate the process of genetic assimilation, which reproduces the qualitative results of available experiments. Our model captures Waddington's picture of developmental paths in a canalized landscape, with alternative paths that can be controlled by either external signals or internal variables. We reconcile this description on the level of individual organisms with the popular description due to Bateman in terms of a population distribution crossing a threshold. Our results suggest the need for more quantitative experiments to study Waddington's ideas of canalization, epigenetic landscape, and genetic assimilation, which have important implications for the direction and speed of evolution.