Introduction

The evolution of sleep has been the subject of several studies and reviews (Allison & Cicchetti, 1976; Allison & Van Twyver, 1970; Hartse, 1994; Karmanova, 1982; Meddis, 1983; Monnier, 1980; Tauber, 1974). However, corresponding studies on the evolution of wakefulness have been fewer (Esteban, Nicolau, Gamundí, et al., 2005; Nicolau, Akaârir, Gamundí, et al., 2000), despite a number of reasons supporting the greater importance of waking in animal adaptation. First of all, waking and sleep are inseparable, an obvious assertion that, notwithstanding, has been ignored in most reviews (see, for instance, Zepelin, 1994; Zepelin & Rechtschaffen, 1974; Zepelin, Siegel, & Tobler, 2005). These reviews compute correlations between the main traits of sleep and ecological variables while forgetting that high correlations of a given trait with total sleep time also imply high correlations with waking time. The present review proposes a change of paradigm from sleep centeredness to waking centeredness.

Let us give an example of the paradigm change: there might be two possible viewpoints related to the high danger of a particular species' exposure within an environment, namely:

1. Sleep is a dangerous state. Therefore natural selection must have reduced sleep in dangerous environments.

2. Alertness is necessary to cope with danger. Therefore natural selection must have increased waking time in dangerous environments.

The difference between the two alternatives might seem subtle: but the former focuses on sleep as a key adaptive factor, while the latter is waking-centered.

Abstract

It is posited that sleep is a network-emergent property of any viable group of interconnected neurons. Animals ranging from jellyfish to all homeotherms sleep. Biochemical sleep-regulatory events, including cytokines and nuclear factor kappa B (NF-kB), are shared by insects and mammals. It seems likely that these sleep-regulatory events evolved from metabolic-regulatory events and that sleep is a local use-dependent process. Relationships between sleep and tumor necrosis factor (TNF) are used to examine the local use-dependent sleep hypothesis. ATP released during neurotransmission is posited to drive the production and release of cytokines, such as TNF, that, in turn, act within a biochemical sleep homeostat in the short term – via adenosine, nitric oxide, and prostaglandins – to enhance non–rapid-eye-movement (NREM) sleep. In the long term, TNF and other sleep-regulatory substances, via NF-kB activation, enhance expression of receptors such as adenosine A1 and glutamate amino-3-hydroxy-5-methylisoxazoleproprionic (AMPA) receptors. Changes in the expression of these receptors will change the sensitivity of neurons and thereby change synaptic efficacy. Such actions suggest that sleep mechanisms cannot be separated from a connectivity function of sleep at the local network level. The need for sleep is derived from the experience-driven changes in neuronal microcircuitry that necessitate the stabilization of synaptic networks to maintain physiological regulatory networks and instinctual and acquired memories. The need for unconsciousness is derived from the local use-dependent sleep mechanisms.

Introduction

Sleep has been detected in every animal that has been adequately studied (Cirelli & Tononi, 2008). The ubiquitous nature of sleep suggests that it evolved early in the course of evolution and therefore may serve a conserved function essential to all animals. This hypothesis forms the rationale behind the development of “simple” animal models of sleep (Allada & Siegel, 2008; Mignot, 2008). By studying sleep in animals such as the fruit fly (Drosophila melanogaster), where the power of genetic techniques can be readily employed, we may gain insight into the initial (perhaps cellular) function of sleep, a function that may still be relevant to understanding sleep in humans. Indeed, recent studies have already demonstrated remarkable similarities between sleep in Drosophila and sleep in mammals (Hendricks, Finn, Panckeri, et al., 2000; Shaw, Cirelli, Greenspan, et al., 2000; reviewed in Cirelli & Bushey, 2008). Although the utility of studying sleep in “simple” animal models is undeniable, it is unlikely that this approach alone will tell the whole story, especially given that Drosophila do not exhibit brain states comparable to mammalian slow-wave sleep (SWS) and rapid eye-movement (REM) sleep (Cirelli, 2006; Cirelli & Bushey, 2008; Hendricks & Sehgal, 2004; Nitz, van Swinderen, Tononi, et al., 2002). Indeed, the heterogeneous nature of mammalian sleep suggests that the specific changes in brain activity that accompany SWS and REM sleep might serve secondarily evolved functions not found in simple animals.

Whether all species sleep or meet the common definition of sleep has recently been questioned (Siegel, 2008). In the majority of species that do sleep, however, the evolutionary conservation of DNA elements regulating sleep and its features highlights the physiological importance of this behavior. From an “adaptation” point of view, we would like to think of sleep as solving a problem, just as we do for traits such as eating, drinking, and so on. In such a perspective, the perpetuation of particular sleep genes would have occurred through improved fitness of the individuals with those genes. Clear scientific evidence on this matter, however, is still missing. Historically, the science of sleep has evolved from a key technological innovation: the development of electrophysiological instruments that allow the recording of changes in electrical activity in brain and muscles. Such a phenomenological approach has been successful in providing a practical framework for understanding “how” we sleep, but it has not contributed to solving the question of “why” we sleep.

The year 1953 was an important year for two important research fields: sleep and genetics. The discovery of rapid-eye-movement (REM) sleep at the University of Chicago, announced in Science (Aserinsky & Kleitman, 1953), laid the foundation for modern research on sleep. That same year, from the Cavendish laboratory in Cambridge, UK, Crick and Watson sent their proposal of a structural model of DNA to Nature (Watson & Crick, 1953b).

Introduction

Evolutionary medicine is a relatively new field of inquiry that attempts to apply the findings and principles of evolutionary anthropology and biology to medical disorders (Armelagos, 1991; Cohen, 1989; Nesse & Williams, 1998; Stearns, 1999; Stearns & Koella, 2007; Trevathan, Smith, & McKenna, 1999, 2008; Williams & Nesse, 1991). Although a fair number of medical disorders have been explored from the evolutionary medicine perspective (see the collection of papers in Stearns, 1999, and Trevathan et al., 1999, 2008), sleep disorders have not been among them. This is unfortunate, as application of evolutionary theory to problems of sleep disorders will likely yield significant new insights into both the causes and solutions of all of the major sleep disorders.

In this chapter, we discuss several of these major sleep disorders as well as some of the less common ones. Our choice of which disorders to cover was rather arbitrary: we chose those where, we believe, evolutionary analysis is currently in a position to shed new light on the symptomatology of the disorder as well as on its potential ultimate causes. We were particularly interested in disorders that might also shed light on a potential science of sleep durations.

Why sleep durations? Time spent asleep is one of the most important aspects of sleep, as it is directly linked to the restorative qualities of sleep. If you do not get enough sleep, you do not feel well.

Introduction

Since the dawn of civilization, sleep has fascinated humankind. Myriad treatises and reviews, scientific and nonscientific, have been written in an attempt to explain the phenomenon of sleep, yet none has been comprehensive enough to gain general acceptance. It is now well established that sleep is neither a unitary nor a passive process. Intricate neuronal systems via complex mechanisms are responsible for controlling sleep. This chapter focuses on the evolution of rapid-eye-movement (REM) sleep; for detailed information about other behavioral states, the reader is referred to several comprehensive reviews (Datta & Maclean, 2007; Jones, 2003; Mignot, 2004; Siegel, 2004; Steriade & McCarley, 2005). We begin with a brief description of the discovery of REM sleep and then describe the phylogeny and evolution of REM.

Discovery of REM sleep

The discovery of REM sleep, a major breakthrough, revolutionized the field of sleep research. The process that led to this discovery began in Kleitman's laboratory at the University of Chicago Medical School in 1953. Kleitman and his graduate student Eugene Aserinsky noticed rhythms in eye movements during sleep in humans and linked this to dreaming (Aserinsky & Kleitman, 1953, 1955). Subsequently, Dement and Kleitman (1957) characterized the electroencephalographic (EEG) activity during dreaming in humans, and later Dement (1958) recorded rapid eye movements during sleep in animals. These discoveries established the presence of the non-REM–REM sleep cycle.

Introduction

The primates comprise a diverse group of eutherian mammals, with between some 200 and 400 species, depending on the taxonomic authority consulted (e.g., Corbet & Hill, 1991; Wilson & Reeder, 2005). Most of these species dwell in tropical forests, but primates also thrive in many other habitats, including savannas, mountainous forests of China and Japan, and even some urban areas. Living primates are divided into two groups, the strepsirrhines (lemurs and lorises) and the haplorrhines (monkeys, apes, and tarsiers). Strepsirrhines include mostly arboreal species and retain several ancestral characteristics, including greater reliance on smell and (in most species) a dental comb that is used for grooming. Most are nocturnal, but some have, in parallel with most haplorrhines, evolved a diurnal niche. They are found only in the Old World tropics. Haplorrhines are more widely distributed geographically, being found in both the New and Old Worlds. They include two groups, the platyrrhines and the catarrhines. Platyrrhines are monkeys native to the New World. Catarrhines include both Old World monkeys and apes. With the exception of owl monkeys in the genus Aotus, all monkeys and apes are active during the day (i.e., diurnal), and most live in bisexual social groups that vary in size from 2 to well over 100 adults (Smuts, Cheney, Seyfarth, et al., 1987).

Nonhuman primates are among the best-studied of mammals, in large part because of their close phylogenetic relatedness to humans.

Introduction

Aquatic habitats were the cradle of sleep many million years before sleep evolved in terrestrial animals. Yet these habitats were the last to be explored in seeking sleep's ultimate function, which I have suggested to be the enabling of highly efficient brain operation at all times. Although the sleep of most fishes is essentially indistinguishable from that of terrestrial vertebrates, by exploiting the rich variety and greater permissiveness of aquatic habitats, some fishes have bypassed a need for sleep. In three continuously active states, they purportedly achieve comparable, and even greater, benefits than is provided by sleep, yet remain perpetually vigilant.

I propose that “schooling” (swimming synchronously in polarized groups) by these fishes plays a major role in the lack of a need for sleep. Thus, by schooling, they are able to achieve sleep's benefits without closing or occluding their eyes, namely, a great reduction in the average school member's reception and processing of external sensory input. Because the evident benefits of schooling by some fishes substitute for the obscure benefits of sleep by closely related fishes, the evident benefits give clues to the obscure ones. These clues support views on the ultimate function of sleep.

After reviewing circumstances relating to the evolution of sleep in terrestrial animals, relevant topics in the lives of fishes are treated, emphasizing their sleep and its awake, almost equivalent functions with eyes open.

Introduction: sleep and ecology

All mammals so far studied experience some form of sleep. When mammals are sleep-deprived, they generally attempt to regain the lost sleep by exhibiting a “sleep rebound,” suggesting that sleep serves important functions that cannot be neglected (Siegel, 2008; Zepelin, 1989; Zepelin, Siegel, & Tobler, 2005). When sleep deprivation is enforced on individuals, it is accompanied by impaired physiological functions and a deterioration of cognitive performance (Kushida, 2004; Rechtschaffen, 1998; Rechtschaffen & Bergmann, 2002). In the rat, prolonged sleep deprivation ultimately results in death (Kushida, 2004; Rechtschaffen & Bergmann, 2002). Together, these observations suggest that sleep is a fundamental requirement for mammalian life, and much research has focused on identifying the physiological benefits that sleep provides (Horne, 1988; Kushida, 2004).

Are there also costs associated with sleep? If so, what are the selective pressures that constrain the amount of time that individuals can devote to sleep? Sleep is probably associated with “opportunity costs” because sleeping animals cannot pursue other fitness-enhancing activities, such as locating food, maintaining social bonds, or finding mates. Sleeping animals may also pay direct costs. For example, sleep is a state of reduced consciousness, and thus sleeping individuals are less able to detect and escape from approaching predators (Allison & Cicchetti, 1976; Lima, Rattenborg, Lesku, et al., 2005). These ecological factors are likely to be important constraints on sleep durations and may also affect how sleep is organized over the daily cycle.