Evolution of self-sustained circadian rhythms is facilitated by seasonal change of daylight

Self-sustained oscillation is a fundamental property of circadian rhythms and has been repeatedly tested since the early days of circadian research, resulting in the discovery of almost all organisms possessing self-sustained circadian oscillations. However, the evolutionary advantage of self-sustainability has been only speculatively discussed. In this theoretical study, we sought the environmental constraints and selection pressure that drive the acquisition or degeneration of self-sustainability through the process of evolution. We considered the dynamics of a gene regulatory network having a light input pathway under 12 h light and 12 h dark cycles or multiple day length conditions and then optimized the network structure using an evolutionary algorithm. By designing the fitness function in the evolutionary algorithm, we investigated the environmental conditions that led to the evolution of the self-sustained oscillators. Then, we found that self-sustained oscillation is rarer than damped oscillation and hourglass-type behaviour. Moreover, networks with self-sustainability have a markedly high fitness score when we assume that a network has to generate a constantly periodic expression profile regardless of day length. This study is, to our knowledge, the first to show that seasonality facilitated the evolution of the self-sustained circadian clock, which was consistent with empirical records.