Seasonal cycles select for self-sustained circadian oscillators.

Circadian clocks are phylogenetically widespread timekeeping mechanisms that provide a fitness-enhancing ability to anticipate time-of-day changes in the environment.1,2,3 A ubiquitous and defining feature of all circadian clocks is their ability to maintain self-sustained oscillations in constant conditions (i.e., constant temperature and constant light or constant darkness), despite the fact that they evolved on Earth, where constant environments are almost unknown.4,5 Damped circadian oscillators can entrain competently to daily light/dark cycles, and even “hourglass” timers can provide temporal order in many environments.6 So, why has the self-sustained property of daily timekeepers been so universally selected to the extent that it is a defining property of circadian systems? An extensive modeling analysis of this question concluded that the daily and seasonal variability of environmental fluctuations in both weather (e.g., temperature, light intensity) and seasonal daylength together demanded self-sustained clocks.7 However, our experimental analysis of this investigation, based on competition among strains expressing differing phenotypes,2,3,5 revealed that changing photoperiods, such as those encountered over the annual cycle of seasons, are a sufficient environmental pressure to select for self-sustained circadian oscillators, even in the absence of fluctuations in other environmental factors. The salient properties of daily circadian clocks are therefore molded by modulations of environmental cycles of multiple periodicities, both daily and annual/seasonal.