Phylogeny

It is believed that the common tetrapod ancestor of birds, mammals, and reptiles displayed a primitive sleep form that did not have distinct REM/SWS states. Following divergence from this common ancestor, two independent evolutions of REM/SWS in birds and terrestial, placental mammals from primitive sleep forms occurred (26). This hypothesis is based on a phyologeny of tetrapods, updated to integrate molecular phylogenies, as presented by Meyer (2003) (Figure 1):

Figure 1. The phylogenetic relationship of tetrapods. From reference 15.

 

The evolution of REM sleep is concurrent with the evolution of SWS sleep; it is believed from studies on 'primitive' mammals like the echidna that REM/SWS coevolved as a differentiation of a sleep behavior that contained elements of both (29).

Characterizing the ancestral primitive sleep form (equivalent to the primitive sleep forms believed to be used by reptiles, amphibians, and fish) as unihempsihperic or non-unihemispheric can be tricky. Assaying unihemispheric sleep is a difficult task; direct demonstration of the presence of unihemispheric sleep requires simultaneous EEG recordings from both hemispheres in sleeping (behaving) animals. Using unilateral eye closure concurrent with the typical behavioral signals of sleep as a behavioral correlate of unihemispheric sleep makes identifying unihemispheric sleep easier, but may be misleading. Reptiles display unilateral eye closure behavior, during both sleep and more active states. However, reptiles lack SWS, and may be closing one eyelid at a time to prevent water loss through the eye (23). It is not clear whether the ancestral sleep form is unihemispheric; it seems safe to assume that it contains aspects of unihemispheric SWS, just as it contained aspects of REM/SWS, but was not truly unihemispheric SWS.

 

Two Major Clades: Birds and Marine Mammals

Unihemispheric sleep, defined as unihemispheric SWS (USWS) that has been demonstrated by EEG, has been idenitfied in two major phylogenetic groups: birds and marine mammmals.

 

Birds

Recorded observations of birds closing one eye at a time during sleep date back to at least 1386, when Geoffrey Chaucer in the prologue to the Canterbury Tales noted:

"And smale fowles...slepen al the night with open yë" (23)

The closing of one eye was not known to be associated with hemishperic asymmetries until Spooner (1964) demonstrated it in the domestic chicken (Gallua gallus domesticus) (31). Subsequently, Japanese quail (Coturnix japonica), Glaucous-winged gull (Larus glaucescens), Mallard (Anas platyrhynchos), and pigeon (Columba livia) have all been shown to have asymmetric EEG activity coupled with unilateral eye closure (UEC). The UEC was correlated with the EEG asymmetry, with the contralateral eye closing during periods of USWS (24). In European blackbirds (Turdus merula), asymmetric EEG activity during sleep has been recorded, but the experimental design prevented simultaneous monitoring of eye closure, making it difficult to ascertain the presence or correlation of UEC (32). While hemispheric asymmetries have not been shown in other birds, UEC has been demonstrated in 29 species, across 13 to 15 (20, 23) orders. The orders that have been observed displaying UEC cover a wide range of the class of birds: social and solitary, terrestrial and aquatic, lateral and frontal facing eyes, and lateral and diurnal. However, UEC is not general to all birds: cuckoos, hummingbirds, swifts, and flightless ratities (e.g. emus) do not display UEC, although no EEG recordings have demonstrated that they do not sleep unihemispherically (23). For a comprehensive list of the known sleep behaviors of birds, see Rattenborg 2000 (23).

The variety of birds that display USWS (or UEC) suggests that the behavior is widespread in across the bird taxa. The generality supoprts the hypothesis that a common avain ancestor displayed USWS. In fact, theories (23) have been proposed that because the theropod dinosaurs (bipedal predators) are similar to birds in many morphological traits (28) they may have been unihemispheric sleepers.

 

Marine Mammals

In 1972, EEG recordings from the pilot whale (Globicephala scammoni) provided the first electrophysiological evidence of differences between the hemispheres during sleep, but this was classified as a relaxed wakefulness, not as USWS. Mukhametov et al (1977) were the first to recognize the asymmetry in hemispheric activity during the sleep of cetaceans (i.e. dolphins) as USWS (17). USWS has been identified, with UEC, in other marine mammalian taxa, such as eared seals (Callorhinus ursinus and Arctocephalus pursillus) and Amazonian manatees (Trichechus inunguis). For a complete list of the known sleep behaviors of marine mammals, see Table 1 below.

 

Table 1. Sleep characteristics of marine mammals. Key: USWS = unihemispheric slow wave sleep; BSWS = bihemispheric slow wave sleep; REM = rapid eye movement; UEC = unilateral eye closure; + = present; - = absent; blank = no data. From reference 23.

 

The mammals that display USWS are placental mammals. The other mammals, marsupials and monotremes, have not been shown to display USWS or UEC; nor have other placentals. Further, Table 1 shows that only a subset of the seals display USWS. It is not clear whether true seals have lost USWS or eared seals have independenly (from birds) evolved USWS; this direction of evolution of USWS in seals depends on the overall phylogeny of the seals, which is not worked completely out.