By Robert Deyes
When I first picked up neurobiologist Jerome Siegel's recent Nature review on the evolutionary significance of sleep, I was expecting to find a scientifically-buttressed counter-position to the age-old assertion that describes sleep as "a vulnerable state...incompatible with behaviors that nourish and propagate species". Siegel's evolutionary discussion was nonetheless unconvincing (1). While he supplied a nice primer on the neurobiology of sleep, Siegel gave no real riposte to the outstanding question of survivability posed above other than to iterate a rather uninformative statement: "In each species the major determinant of sleep duration is the trade-off between the evolutionary benefits of being active and awake and those of adaptive inactivity" (1).
To understand why Siegel fell short it is important to re-familiarize ourselves with the rich diversity of sleep behaviors that we find in the mammalian world. Children learn about these behaviors from an early age: giraffes nap for anywhere between 10 minutes to two hours, elephants for five hours and anteaters for as long as fourteen hours (2). Marine mammals exhibit their own unique sleep patterns, notably a unilateral (unihemispheric) slow down of brain wave activity (contrast this with the bilateral (bihemispheric) slow down of non-REM sleep in land mammals) (1,3). And seals make use of both bilateral and unilateral modes depending on whether they are in terrestrial or aquatic environments (1,3). Researchers readily proclaim that "mammalian sleep is extremely diverse" with the unihemispheric sleep of dolphins being "nothing like the rapidly cycling sleep of rodents, or the single daily block of humans" (3).
While a direct correlation between body mass and sleep quantity has been reported in herbivores, the impact of mass and other physiological variables on sleep patterns across the animal kingdom remains highly controversial (1). Moreover there appear to be significant mammalian species-specific differences regarding the lethality of sleep deprivation as well as in hormone release patterns during sleep and wake times (1). In all three subclasses of mammals (placentals, marsupials and monotremes) there are noticeable differences in REM/NON-REM sleep patterns. Extant monotremes for example are unique in their display of brainstem associated REM and forebrain Non-REM (1).
Many mammals and several invertebrate species can regain lost sleep (sleep rebound) in about 30% less time than it would have taken during their normal sleep routine (1). Understandably evolutionists have pondered over the question of why in such cases shorter sleep durations and concomitantly longer wake times have not evolved so as to maximally capitalize on opportunities for hunting and foraging (1). Strikingly dolphins, killer whales and seals can survive the winter months without sleep rebound after extended periods of activity in the open sea (1). In all, these results are at odds with the expectation that sleep would be "physiologically similar across mammals" (1).
Speculation over why animals would spend significant portions of their lives in vulnerable states of dormancy has focused on the benefits of brain energy conservation and the concomitant reduced risks of injury and detection by predators. Siegel defined the adaptive benefits of sleep as the suppression of activity at times that have "maximal predator risk and minimal opportunity for efficiently meeting vital needs" and the allowance of activity at times of "maximal food and prey availability and minimal predator risk" (1). Yet in light of the rather complex and varied sleep behavior patterns described thus far, Siegel's conclusions seem empirically un-testable. How can we truly ascertain whether some poorly defined threshold of ill-timed predatory risks and inefficient brain energy conservation has been reached?
If anything real life observations contravene expectations. A few examples make this plainly clear: the 19th century zoologist James Edward Gray recorded crossing paths with bowhead whales "sleeping so soundly a few meters from the pack ice that they did not even react to his approaching boat" (4). Owls are prone to large mob lynchings from hawks, crows and jays as they doze atop exposed tree trunks (5). Humming birds make themselves susceptible to attack by adopting an almost lifeless state called torpor as part of an energy-recovery sleep regimen (3). And mortality in certain reef teleost fish is higher during the night when resting than during the day when swimming in open waters (6). Such life-threatening vulnerabilities do not support the existence of trade-offs acting as effective evolutionary operatives over the course of time as Siegel might have envisaged.
World-renowned biochemist James Krueger concurs- sleep is by all counts maladaptive unless "a greater need is served" (7). What that need might be remains to be seen although there is no shortage of ideas. Krueger for example believes that sleep may somehow facilitate the integration of new memories into existing neuronal circuits (7). Some speculate that sleep serves the role of removing dangerous free radicals from the brain . Others hold to the veracity of the Null Hypothesis which, simply stated, maintains that sleep is nothing more than "a kind of extreme indolence that animals indulge in when they have no more pressing needs, such as eating or reproducing" . Sleep quite clearly performs a restorative function although the exact details have eluded even the most dedicated of investigative minds . In what way can the current data be reconciled with a picture that shows sleep behaviors evolving as a result of selective pressures across the millennia?
In the June, 2010 issue of PLOS Computational Biology, a cross-disciplinary group from the University of Sydney and Harvard Medical School headed by Amesh Abeysuriya provided what was touted as the definitive answer to this question (3). At the heart of mammalian sleep behaviors is a collection of diverse molecules called somnogens that accumulate during wake times and generate a "homeostatic drive to sleep". Cells in the monoaminergic brainstem nuclei (MA) and the ventro lateral preoptic area of the hypothalamus (VLPA) form what Abeysuriya et al consider to be a sleep-wake switch that functions through antagonistic inhibition (3). For aquatic mammals in which unihemispheric activity is observed, a "mutually inhibitory connection" is thought to exist between VLPA populations that prevents both hemispheres being activated simultaneously. Abeysuriya et al devised a model that they claim accounts for the sleep patterns observed in 17 species of mammals (3).
Krueger is one of a handful of sleep experts who believe that sleep is not an "all or nothing" affair even in bihemispheric-operating mammals (9). Krueger has proposed that in all mammals groups of neurons can be selectively shut down after being used for the tasks they routinely perform (4). What we call sleep might therefore simply be a state in which a large number of neurons have been shut down to the extent that they are no longer able to function (9). Washington State University electrophysiologist David Rector has built up enough hard evidence to support such a proposal. Following experiments with lab rats Rector is confident that "there's no central control, no on-off switch". He remains adamant that the need for sleep arises as a result of the progressive use of neuronal cell clusters over the course of a wake period (9).
Several somnogens have now been extensively reported on in the peer-reviewed literature (3). The universality of the homeostatic drive that results from these somnogens coupled with the MA-VLPA cellular interactions have led Abeysuriya et al to conclude that differences in sleep patterns across species represent nothing more than evolutionary attenuations of a system that existed before mammals roamed the earth (3). But blatantly lacking in this evolutionary picture is a genetic basis for explaining how these attenuations supposedly came into effect. Ever since the early 1970s, when researchers began a frantic search for a mysterious sleep hormone dubbed "Factor S", the idea of a single sleep gene has been gradually but emphatically turned on its head (7,9). There are now over a hundred such genes, most of them encoding a class of immune proteins called cytokines, that in one way or another play a role in regulating sleep patterns (7,9). Of these there are about fifteen big players with TNF, IL-1, Growth Hormone Releasing Hormone (GHRH) and adenosine (with its receptor) being perhaps the best characterized of them all (3,9,10).
A complex network of positive and negative feedback loops called the sleep homeostat forms the molecular foundation of non-REM phase sleep which varies predictably in response to physiological cues such as feeding and illness (10). Importantly Krueger's research has brought into sharp clarity the role of a gene called preproghrelin which is now known to modulate sleep and regulate body temperature as a function of food availability (11). The preproghrelin gene expresses multiple protein products one of which, the ghrelin hormone, acts in suppressing sleep during bouts of hunger (11). Another preproghrelin product, the obestatin hormone, induces sleep and maintains stable body temperatures when food is scarce (11). These antagonistic functions are critical for survival in the wild where "natural shortages of food and low environmental temperature are commonly encountered" (12). Indeed preproghrelin gene knockout mice have been shown to suffer from severely disrupted sleep and uncontrollable hypothermia when doubly challenged by an absence of food and cold external temperatures (12)
Any model that purports to explain the evolution of sleep throughout nature has to account for the multi-layered genetic and cellular complexity that undergirds its panoply of forms. Clearly involved are exquisitely regulated and species-tailored communication systems, with key biological processes and molecular determinants playing an integral role in sleep/wake regulation. None of the work to-date on evolution has given us much beyond deeply-held assumptions served up in a manner that leaves out the full extent of what we now truly know about this captivating topic. It can be said that at its core the current evolutionary story has become nothing more than the materialists' dreamy solution to a nightmare of a problem.
1. Jerome M. Siegel (2010) Sleep Viewed As A State Of Adaptive Inactivity, Nature Rev Neurosci, Volume 10, pp. 747-753
2. Richard and Louise Spilsbury, A Herd Of Elephants, Heinemann Library, p.20; Jennifer McDougall, Giraffes, Scholastic, p.25; Lorien Kite, Anteaters, Grolier Educational, p.30
3. Andrew J. K. Phillips, Peter A. Robinson, David J. Kedziora , Romesh G. Abeysuriya (2010) Mammalian Sleep Dynamics: How Diverse Features Arise from a Common Physiological Framework, PLOS Computational Biology, June 2010, Volume 6, Issue 6, e1000826
4. Jacques Cousteau and Yves Paccalet (1986) Whales, W.H. Allen & Co, London, pp. 219
5. Helen Rodney Sattler (1995) The Book Of North American Owls, Clarion Books, NY, p. 23
6. Chiara Cirelli, Giulio Tononi (2008) Is Sleep Essential? PLOS Biology, Volume 6, Issue 8, e216
7. Tim Steury (2010) Why Do We Sleep?, Washington State Magazine, See
8. The New Book Of Popular Science, Volume 5, Grolier Publishing, pp. 405-409
9. Cherie Winner (2006) The Secrets Of Sweet Oblivion, Washington State Magazine, See http://wsm.wsu.edu/s/index.php?id=130
10. James M Krueger, David M Rector, Sandip Roy, Hans P A Van Dongen, Gregory
Belenky, and Jaak Panksepp (2008) Sleep As A Fundamental Property Of Neuronal Assemblies, Nat Rev Neurosci Volume 9, pp. 910-919
11. Eat, sleep, stay warm: How our bodies find the right balance, See
12. Eva Szentirmaia, Levente Kapa, Yuxiang Sun, Roy G. Smith, and James M. Krueger (2009) The preproghrelin gene is required for the normal integration of thermoregulation and sleep in mice, PNAS, Vol. 106, pp.14069-14074
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