Concordance of the circadian clock with the environment is necessary to maximize fitness in natural populations

Abstract

The ubiquity of endogenous, circadian (daily) clocks among eukaryotes has long been held as evidence that they serve an adaptive function, usually cited as the ability to properly time biological events in concordance with the daily cycling of the environment. Herein we test directly whether fitness is a function of the matching of the period of an organism's circadian clock with that of its environment. We find that fitness, measured as the per capita expectation of future offspring, a composite measure of fitness incorporating both survivorship and reproduction, is maximized in environments that are integral multiples of the period of the organism's circadian clock. Hence, we show that organisms require temporal concordance between their internal circadian clocks and their external environment to maximize fitness and thus the long-held assumption is true that, having evolved in a 24-h world, circadian clocks are adaptive.

Figure 1

Resonance experiments. (A) Rhythmic response of Wyeomyia smithii from the Gulf Coast of North America (30–31°N) to light:dark (L:D) cycles ranging from L:D = 10:14–10:62 in separate experiments (Bradshaw et al. 2003). The data are pooled from the two populations used in this study. Note that all of these regimens consist of diapause-maintaining short days and long nights so that the rhythmic long-day response represents rhythmic transitions from resonant cycles producing short-day response “valleys” to nonresonant long-day response “peaks.” The arrows indicate three of the four experimental regimens: (A) L:D = 10:14; (B) L:D = 10:25; (C) L:D = 10:36. (B) Fitness (per-capita expectation of future offspring) in response to the L:D cycles indicated in Figure 1A and to a long-day L:D = 18:6 cycle (L). Error bars represent two standard errors. ***P < 0.001 when comparing L:D = 10:25 with the other three cycles, which did not differ from each other.

Figure 2

Components of fitness: (A) pupal survivorship; (B) average fecundity per female; (C) embryonic viability, and (D) adult longevity, in the four different light treatments (Light:Dark) used in this study. Error bars represent two standard errors. ***P<0.001 when comparing L:D = 10:25 with the other three cycles, which did not differ from each other.