Evolution of temporal order in living organisms

Abstract

Circadian clocks are believed to have evolved in parallel with the geological history of the earth, and have since been fine-tuned under selection pressures imposed by cyclic factors in the environment. These clocks regulate a wide variety of behavioral and metabolic processes in many life forms. They enhance the fitness of organisms by improving their ability to efficiently anticipate periodic events in their external environments, especially periodic changes in light, temperature and humidity. Circadian clocks provide fitness advantage even to organisms living under constant conditions, such as those prevailing in the depth of oceans or in subterranean caves, perhaps by coordinating several metabolic processes in the internal milieu. Although the issue of adaptive significance of circadian rhythms has always remained central to circadian biology research, it has never been subjected to systematic and rigorous empirical validation. A few studies carried out on free-living animals under field conditions and simulated periodic and aperiodic conditions of the laboratory suggest that circadian rhythms are of adaptive value to their owners. However, most of these studies suffer from a number of drawbacks such as lack of population-level replication, lack of true controls and lack of adequate control on the genetic composition of the populations, which in many ways limits the potential insights gained from the studies. The present review is an effort to critically discuss studies that directly or indirectly touch upon the issue of adaptive significance of circadian rhythms and highlight some shortcomings that should be avoided while designing future experiments.

Figure 1

Circadian clocks are essential for survival of organisms under natural conditions. (A) Average survivorship of white-tailed antelope ground squirrels under semi-natural habitats. The animals were released in semi-natural habitat after surgical removal of their supra-chiasmatic nucleus (SCN) based circadian clocks. During the study period three out of five SCN-lesioned (SCN-X) individuals were predated upon as compared to two out of seven control animals. (modified after DeCoursey et al, 1997 [16]) (B) Average survivorship of free-living eastern chipmunks under natural environment. Free-living animals were captured from the study area and released back after surgical ablation of their SCN. The control animals were handled similarly and released back to the study area. During the eighty days of the study, more than 80% of SCN ablated individuals fell prey to weasels while mortality was significantly less in the surgical (sham) and intact controls. (modified after DeCoursey et al, 2000 [17])

Figure 2

Molecular feedback loops of cyanobacteria. A cluster of KaiABC genes controls circadian rhythms in cyanobacteria. KaiA gene product acts as a positive regulator for KaiBC transcription, while KaiBC products along with other proteins inhibit their own transcription.

Figure 3

Interlocked molecular feedback loops of Neurospora. White-collar complex (WCC) acts as the transcriptional activator (positive element) of Frequency gene (Frq). The protein product of Frq undergoes phosphorylation in the cytoplasm under the influence of specific kinases, and subsequently acts as inhibitor of its own transcription (negative element). WCC levels are regulated by another gene called Vivid (Vvd), which in turn is regulated by WCC complex. Thus, WCC acts as one of the key components of Neurospora clock that connects the two loops, and hence appear to be important for the persistence of molecular oscillations. In addition, WCC is light sensitive, and appears to be crucial for light entrainment for the Neurospora molecular clock.

Figure 4

Interlocked molecular feedback loops in Drosophila melanogaster. CLOCK/CYCLE heterodimer acts as transcriptional activator (positive element) for period (per) and timeless (tim) genes. The heterodimer of PER/TIM is phosphorylated in the cytoplasm in the presence of specific kinases, and the phosphorylated complex then acts as inhibitor for its own transcription (negative element). The VRI and PDP1 proteins regulate the levels of CLK/CYC complex, which in turn are regulated by CLK/CYC. Thus, CLK/CYC heterodimer appears to be an important component that connects the two loops and is important for sustaining molecular oscillations. The protein Cryptochrome (CRY) has been implicated in the light entrainment pathways of the Drosophila molecular clock.

Figure 5

Interlocked molecular feedback loops of mammals. CLOCK/ BMAL1 heterodimer acts as the transcriptional activator (positive element) for Period (Per) and Cryptochrome (Cry) genes. The PER/CRY protein complex is phosphorylated in the cytoplasm by specific kinases, which then acts as inhibitor for their own transcription (negative element). In addition, these heterodimers activate Bmal1 transcription. CLK/BMAL1 transcription is inhibited by REV-ERBα, which in turn is regulated by CLK/BMAL1. Thus, CLK/BMAL1 heterodimer appears to be one of the key components of mammalian molecular clock, which connects the two loops. The Period1 gene product (PER1) is light-sensitive and appears to be important for the light entrainment of mammalian molecular clock.

Figure 6

Circadian resonance in cyanobacteria. Rhythmic strains having different free-running periods were competed under LD cycles of different lengths. Strains whose free-running period matched that of LD cycles out-competed those with deviant periods. Middle panels represent initial composition of the competing strains. Values in the parenthesis indicate the free-running period of the cyanobacterial strains. (Figure modified after Ouyang et al, 1998 [6])

Figure 7

Competition between rhythmic and arrhythmic strains of cyanobacteria. Mutant strains with arrhythmic (CLAc), or dampened (CLAb) bioluminescence rhythm, as well as the rescued strains were competed against wild type strain under periodic and constant environments (LD cycles and LL, respectively). Rhythmic strains out competed the wild type strain under LD cycles, but the arrhythmic strains out competed rhythmic strains under LL. Middle panels represent initial composition of the competing strains. Values in the parenthesis indicate the free-running period of the cyanobacterial strains. (Figure modified after Woelfle et al, 2004 [97])