The adaptive value of circadian systems: a review of a review

Well, it's been one year now. No, not just for Tangled Bank, but more importantly for me: it's been a year since I defended my thesis! To celebrate, I'll steer this blog temporarily away from politics and satire to actual science stuff: stuff that I've kinda wondered about for a while. Stuff that actually appears in the introduction of my thesis:

"It is thought that a selective evolutionary advantage that has been passed down to humans is conferred by the ability to express circadian rhythms and synchronize these with environmental stimuli..."

[yes, my sentences are as long, winding, and boxy in my thesis as they are in my blog].

It seems as though in the field of circadian rhythms one truth many hold to be self-evident is that the circadian clock confers some kind of evolutionary advantage onto species that have a functioning one. As Circadiana does a much better job describing, the internal circadian clock is an endogenous pacemaker that keeps approximate 24-hour time. This happens all on its own, without inputs from the surrounding environment such as light. The clock transmits its temporal information to other parts of the brain to help synchronize events that ought to occur at distinct times of the 24-hour cycle. Since a number of important physiological functions are coordinated by the clock and since most species express a circadian rhythm, many of us in the field would like to believe that circadian rhythms are important evolutionarily. The argument goes something like this: if everything from single-celled organisms to humans express an endogenous rhythm that happens to be close to the average 24-hour day-night cycle, why would that not have been an evolutionarily important trait? Well, this review by Carl Johnson (Methods Enzym., 393:818-837, 2005) addresses some really fundamental questions about the assertion that circadian rhythms were selected for evolutionarily. Namely, if rhythmicity is so important, can we show that its presence enhances reproductive fitness? As a non evolutionary biology coming from the field of circadian rhythms, this is quite fascinating to me. Put in Johnson's words:

...many biological phenomena might have evolved (1) as a random trait that was neither adaptive nor nonadaptive, (2) as a trait physiologically linked to another trait where the linkage is either not currently present or not obvious, (3) as a trait that was once adaptive, but is no longer (e.g., the appendix of humans), (4) as a trait that evolved for one purpose but later was recruited to another task, and so on. To illustrate the concept, consider the case of human noses and spectacles—because noses provide such an excellent platform for mounting spectacles, it would be easy to assume in the absence of knowledge of the history of noses and spectacles that noses evolved so as to provide a place for spectacles to reside.

He then goes on to site the same author I sited in the previous quote from my thesis: DeCoursey, 2004. (In: Dunlap, J.C., Lords, J.J. and DeCoursey, P.J., Editors, 2004. Chapter 2 in "Chronobiology: Biological Timekeeping", Sinauer, Sunderland, MA, pp. 27–65.) Johnson argues that the proper use of the definition of fitness is important:

"Fitness is a measure of reproductive success and the passing on of genes. Fitness may be influenced by longevity, survival, growth, development, and other factors, but these ancillary factors are not direct measures of fitness. For example, consider the case of a mighty but sterile lion (an example told to the author by Michael Menaker in an introductory biology class). This lion might dominate a pride and survive to a ripe old age, but it is the wimpy but fertile lion that skulks in the shadows, surreptitiously inseminating the lionesses, who will pass his genes to the next generation.

Reproductive success is the key when asking about fitness: can endogenous 24-hour rhythms enhance the ability of an organism to reproduce? And the definition of adaptation must also be kept clearly in mind when pondering this question:

"An adaptation is an aspect of the phenotype that is the product of evolution by natural selection in a particular environmental context and represents a solution to some challenge presented by the environment. In this sense, an adaptation is a feature of an organism that enhances its reproductive success relative to other possible features (Futuyma, 1998). However, the process of adaptation refers to ongoing phenotypicgenetic evolutionary change driven by natural selection in a given environmental context. So an adaptation is the result of the process of adaptation.
Strictly speaking, an adaptation can only be assumed to be adaptive when it first appears."

When it comes to the evolutionary value of circadian rhythms it is important to remember that the circadian clock must somehow directly influence the ability of an animal to survive up until the time it is capable of reproducing. Not only that, changes in the environment must be able to affect changes in the internal clock mechanism that allow for greater reproductive fitness. Johnson further states:

"The original adaptation of circadian clocks was presumably to enhance reproductive fitness in natural environments, which are cyclic (24h) conditions. We can refer to this situation as an adaptation to extrinsic conditions. However, some researchers have proposed that circadian clocks may additionally provide an "intrinsic" adaptive value (Klarsfeld 1998; Paranjpe 2003 and Pittendrigh 1993). That is, circadian pacemakers may have evolved to become an intrinsic part of internal temporal organization and, as such, may have become intertwined with other traits that influence reproductive fitness in addition to their original role for adaptation to environmental cycles. Note that a rigorous evolutionary biologist would no longer consider an intrinsic value for clocks to be an adaptation if their original extrinsic value has been lost. However, if clocks retain extrinsic value and additionally accrue intrinsic value, then they would still be considered an adaptation."

With these definitions in mind, Johnson reviews the literature (pre-1980 and post-1980) with a view towards how one can measure the adaptive value of circadian clocks in evolution. The pre-1980 dogma that total survival time estimates a trait's adaptive value (broadly speaking) is somewhat incomplete in this sense since an animal can be impotent and survive until a very old age. Post-1980, Johnson reviews much of his own work--he has thought long and deep about the subject--in which he directly tests his hypotheses on cyanobacteria and actually finds evidence for an adaptive value of circadian rhythms in cyanobacteria. Finally, his review wraps up with thoughts about how this might translate to so-called "higher" organisms. He briefly reviews the work of DeCoursey et al. (2000, J. Comp. Physiol. A. 186, pp. 169–180), in which she took chipmunks living in the wild and either lesioned their circadian clock (the suprachiasmatic nucleus or "SCN" of the brain) or sham-operated the animals before placing them back in their home dens.

"The major behavioral difference between SCN-X chipmunks and sham-control groups observed in this study was an increase of the nighttime activity of the animals in their dens ( DeCoursey et al., 2000). DeCoursey et al. (2000) concluded that this nocturnal restlessness allowed the weasel predator to detect the chipmunks (by vibration or other cues) and descend into the burrows to capture and kill the prey. For circadian biologists, these results were both a delight and a surprise. The delight was that the results confirmed the importance of the SCN and, by implication, the clock (perhaps the SCN has important nonclock functions, however?). The surprise was that predation seemed to cue on nocturnal restlessness rather than the phasing of surface activity. One might imagine that a simple system could adequately prevent nocturnal restlessness without the necessity to elaborate a circadian clock with entrainment capability. Is it really true that the function of the clock regulating chipmunk activity is merely to suppress nighttime activity? If so, does this mean that the oft-hypothesized purpose of the circadian clock to anticipate daily environmental events is another "just-so" story? Of course, natural selection builds on preexisting characteristics, and it is possible that natural selection enlisted a circadian mechanism that originally evolved to satisfy more stringent specifications in order to accomplish a plebian task in chipmunks—to suppress nocturnal activity."

So, they survived longer with SCNs (their circadian clock) intact than when it was ablated, but that doesn't necessarily mean they were more likely to reproduce--at least not in the timeframe the experiments could determine. Presumably, younger animals without a clock might not survive to reproductive age. There seems to also be a deeper question Johnson wants to bring out here. Namely, if the only reason the circadian clock is there for is to stop animals from being active during the day (nocturnal) or night (diurnal), why's it gotta be so complicated? That makes me wonder if a.) it's not really all that complicated and b.) it needs to be an internal clock so that it can run on its own regardless of lighting conditions.

First off: is the circadian clock really that complicated? The place in the brain where the clock is located in mammals--the suprachiasmatic nucleus or SCN--is actualy quite a small area comprising only about 20,000 cells total in rodents (miniscule as far as brain areas go). This area receives input from the outside world--mainly from the retina--and transmits information to surrounding brain areas through relatively straightforward synaptic (and non-synaptic) mechanisms. Inside the SCN, most cells express their own rhythm--which can be measured in various ways--and they coordinate their rhythms with one another. The "gears" of the clock are composed of a half-dozen or so core clock molecules that alternate in positive and negative feedback loops and ultimately determine the state that each cell is in. OK, that's complex and there's lots to learn, but it still seems rather simple to me compared to other brain functions. I think it's rather plausible, as Johnson states later on in that section, that the mammalian system built on preexisting features, even if we can now only recognize one rather "plebian" task circadian rhythms are associated with in chipmunks.

Secondly, we cannot be sure if the fact that the system runs the way it does didn't help the chipmunk establish itself in its environment in the first place. Maybe a system that is both continuously cycling on its own and is able to respond to extermal lighting situations actually helped the chipmunk--and other species--expand in latitude as well as longitudinally. The needs of a rodent in terms of internal clock vs external cues are far different in Florida than in Alaska, something which Johnson also addresses later in the review.

The review ends with a discussion on how circadian clocks might have originally (i.e. in cyanobacteria) been used to "escape from light" and a discussion on future directions of research. I am probably in over my head in discussing evolution--my bread and butter is electrophysiology--and I welcome comments from evolutionary biologists and anyone else who might wander by. But for me, this is really a fascinating issue raised in Johnson's review and the numerous works he cites because it ponders some of the deepest thoughts on the wherefore of the system we are studying as circadian biologists. I also believe it's a valuable thought game to have in any field of neuroscience and biology. Lastly, it points out how important rigorous evolutionary biology training is to any field in biology.