David R. Samson

Chimpanzees Preferentially Select Sleeping Platform Construction Tree Species with Biomechanical Properties that Yield Stable, Firm, but Compliant Nests

The daily construction of a sleeping platform or “nest” is a universal behavior among large-bodied hominoids. Among chimpanzees, most populations consistently select particular tree species for nesting, yet the principles that guide species preferences are poorly understood. At Semliki, Cynometra alexandri constitutes only 9.6% of all trees in the gallery forest in which the study populations ranges, but it was selected for 73.6% of the 1,844 chimpanzee night beds we sampled. To determine whether physical properties influence nesting site selection, we measured the physical characteristics of seven common tree species at the Toro-Semliki Wildlife Reserve, Uganda. We determined stiffness and bending strength for a sample of 326 branches from the seven most commonly used tree species. We selected test-branches with diameters typically used for nest construction. We measured internode distance, calculated mean leaf surface area (cm2) and assigned a tree architecture category to each of the seven species. C. alexandri fell at the extreme of the sample for all four variables and shared a tree architecture with only one other of the most commonly selected species. C. alexandri was the stiffest and had the greatest bending strength; it had the smallest internode distance and the smallest leaf surface area. C. alexandri and the second most commonly selected species, Cola gigantea, share a ‘Model of Koriba’ tree architecture. We conclude that chimpanzees are aware of the structural properties of C. alexandri branches and choose it because its properties afford chimpanzees sleeping platforms that are firm, stable and resilient.

Hadza sleep biology: Evidence for flexible sleep‐wake patterns in hunter‐gatherers

OBJECTIVES Cross-cultural sleep research is critical to deciphering whether modern sleep expression is the product of recent selective pressures, or an example of evolutionary mismatch to ancestral sleep ecology. We worked with the Hadza, an equatorial, hunter-gatherer community in Tanzania, to better understand ancestral sleep patterns and to test hypotheses related to sleep segmentation. METHODS We used actigraphy to analyze sleep-wake patterns in thirty-three volunteers for a total of 393 days. Linear mixed effects modeling was performed to assess ecological predictors of sleep duration and quality. Additionally, functional linear modeling (FLM) was used to characterize 24-hr time averaged circadian patterns. RESULTS Compared with post-industrialized western populations, the Hadza were characterized by shorter (6.25 hr), poorer quality sleep (sleep efficiency = 68.9%), yet had stronger circadian rhythms. Sleep duration time was negatively influenced by greater activity, age, light (lux) exposure, and moon phase, and positively influenced by increased day length and mean nighttime temperature. The average daily nap ratio (i.e., the proportion of days where a nap was present) was 0.54 (SE = 0.05), with an average nap duration of 47.5 min (SE = 2.71; n = 139). DISCUSSION This study showed that circadian rhythms in small-scale foraging populations are more entrained to their ecological environments than Western populations. Additionally, Hadza sleep is characterized as flexible, with a consistent early morning sleep period yet reliance upon opportunistic daytime napping. We propose that plasticity in sleep-wake patterns has been a target of natural selection in human evolution.

Shining Evolutionary Light on Human Sleep and Sleep Disorders

Sleep is essential to cognitive function and health in humans, yet the ultimate reasons for sleep—i.e. ‘why’ sleep evolved—remain mysterious. We integrate findings from human sleep studies, the ethnographic record, and the ecology and evolution of mammalian sleep to better understand sleep along the human lineage and in the modern world. Compared to other primates, sleep in great apes has undergone substantial evolutionary change, with all great apes building a sleeping platform or ‘nest’. Further evolutionary change characterizes human sleep, with humans having the shortest sleep duration, yet the highest proportion of rapid eye movement sleep among primates. These changes likely reflect that our ancestors experienced fitness benefits from being active for a greater portion of the 24-h cycle than other primates, potentially related to advantages arising from learning, socializing and defending against predators and hostile conspecifics. Perspectives from evolutionary medicine have implications for understanding sleep disorders; we consider these perspectives in the context of insomnia, narcolepsy, seasonal affective disorder, circadian rhythm disorders and sleep apnea. We also identify how human sleep today differs from sleep through most of human evolution, and the implications of these changes for global health and health disparities. More generally, our review highlights the importance of phylogenetic comparisons in understanding human health, including well-known links between sleep, cognitive performance and health in humans.

Segmented sleep in a nonelectric, small-scale agricultural society in Madagascar

We studied sleep in a rural population in Madagascar to (i) characterize sleep in an equatorial small‐scale agricultural population without electricity, (ii) assess whether sleep is linked to noise levels in a dense population, and (iii) examine the effects of experimentally introduced artificial light on sleep timing.

What is segmented sleep? Actigraphy field validation for daytime sleep and nighttime wake

OBJECTIVE To compare different scoring parameter settings in actigraphy software for inferring sleep and wake bouts for validating analytical techniques outside of laboratory environments. DESIGN To identify parameter settings that best identify napping during periods of wakefulness, we analyzed 137 days on which participants reported daytime napping, as compared with a random subset of 30 days when no naps were reported. To identify settings that identify periods of wakefulness during sleep, we used data from a subsample of women who reported discrete wake bouts while nursing at night. SETTING Equatorial Tanzania in January to February 2016. PARTICIPANTS The Hadza-a non-industrial foraging population. MEASUREMENTS Thirty-three subjects participated in the study for 393 observation days. Using the Bland-Altman technique to determine concordance, we analyzed reported events of daytime napping and nighttime wake bouts. RESULTS Only 1 parameter setting could reliably detect reported naps (15-minute nap length, ≤50 counts). Moreover, of the 6 tested parameter settings to detect wake bouts, the setting where the sleep-wake algorithm was parameterized to detect 20 consecutive minutes throughout the designated sleep period did not overestimate or underestimate wake bouts, had the lowest mean difference, and did not significantly differ from reported wake-bout events. CONCLUSION We propose operational definitions for multiple dimensions of segmented sleep and conclude that actigraphy is an effective method for detecting segmented sleep in future cross-site comparative research. The implications of such work are far reaching, as sleep research in preindustrial and developing societies is documenting natural sleep-wake patterns in previously inaccessible environments.

The evolution of human sleep: Technological and cultural innovation associated with sleep-wake regulation among Hadza hunter-gatherers

Sleep is necessary for the survival of all mammalian life. In humans, recent investigations have generated critical data on the relationship between sleep and ecology in small-scale societies. Here, we report the technological and social strategies used to alter sleep environments and influence sleep duration and quality among a population of hunter-gatherers, the Hadza of Tanzania. Specifically, we investigated the effects that grass huts, sound levels, and fire had on sleep. We quantitatively compared thermal stress in outdoor environments to that found inside grass hut domiciles to test whether the huts function as thermoregulated microhabitats during the rainy season. Using physiological equivalent temperature (PET), we found that the grass huts provide sleep sites with less overall variation in thermal stress relative to outside baseline environments. We also investigated ambient acoustic measures of nighttime environments and found that sound significantly covaried with sleep-wake activity, with greater sound levels associating with less sleep. Finally, after controlling for ecological variables previously shown to influence sleep in this population, fire was shown to neither facilitate nor discourage sleep expression. Insofar as data among contemporary sub-tropical foragers can inform our understanding of past lifeways, we interpret our findings as suggesting that after the transition to full time terrestriality, it is likely that early Homo would have had novel opportunities to manipulate its environments in ways that could have significantly improved sleep quality. We further conclude that control over sleep environment would have been essential for migration to higher latitudes away from equatorial Africa.

Activity patterns in seven captive lemur species: Evidence of cathemerality in Varecia and Lemur catta?

Cathemerality, or activity throughout the 24‐hr cycle, is rare in primates yet relatively common among lemurs. However, the diverse ecological conditions under which cathemerality is expressed complicates attempts to identify species‐typical behavior. For example, Lemur catta and Varecia have historically been described as diurnal, yet recent studies suggest that they might exhibit cathemeral behavior under some conditions. To investigate this variation, we monitored activity patterns among lemurs that are exposed to similar captive environments. Using MotionWatch 8 ® actigraphy data loggers, we studied 88 lemurs across seven species at the Duke Lemur Center (DLC). Six species were members of the family Lemuridae (Eulemur coronatus, E. flavifrons, E. mongoz, L. catta, V. rubra, V. variegata), while a seventh was strictly diurnal and included as an out‐group (Propithecus coquereli). For each 24‐hr cycle (N = 503), we generated two estimates of cathemerality: mean night (MN) activity and day/night (DN) activity ratio (day and night cutoffs were based on astronomical twilights). As expected, P. coquereli engaged in the least amount of nocturnal activity according to both measures; their activity was also outside the 95% confidence intervals of all three cathemeral Eulemur species, which exhibited the greatest evidence of cathemerality. By these estimates, Varecia activity was most similar to Eulemur and exhibited substantial deviations from P. coquereli (β (MN) = 0.22 ± SE 0.12; β (DN) = −0.21 ± SE 0.12). L. catta activity patterns also deviated from P. coquereli (β (MN) = 0.12 ± SE 0.11; β (DN) = −0.15 ± SE 0.12) but to a lesser degree than either Varecia or Eulemur. Overall, L. catta displayed an intermediate activity pattern between Eulemur and P. coquereli, which is somewhat consistent with wild studies. Regarding Varecia, although additional observations in more diverse wild habitats are needed, our findings support the existence of cathemeral behavior in this genus.

Chronotype variation drives night-time sentinel-like behaviour in hunter–gatherers

Sleep is essential for survival, yet it also represents a time of extreme vulnerability to predation, hostile conspecifics and environmental dangers. To reduce the risks of sleeping, the sentinel hypothesis proposes that group-living animals share the task of vigilance during sleep, with some individuals sleeping while others are awake. To investigate sentinel-like behaviour in sleeping humans, we investigated activity patterns at night among Hadza hunter–gatherers of Tanzania. Using actigraphy, we discovered that all subjects were simultaneously scored as asleep for only 18 min in total over 20 days of observation, with a median of eight individuals awake throughout the night-time period; thus, one or more individuals was awake (or in light stages of sleep) during 99.8% of sampled epochs between when the first person went to sleep and the last person awoke. We show that this asynchrony in activity levels is produced by chronotype variation, and that chronotype covaries with age. Thus, asynchronous periods of wakefulness provide an opportunity for vigilance when sleeping in groups. We propose that throughout human evolution, sleeping groups composed of mixed age classes provided a form of vigilance. Chronotype variation and human sleep architecture (including nocturnal awakenings) in modern populations may therefore represent a legacy of natural selection acting in the past to reduce the dangers of sleep.

Sleep in a comparative context: Investigating how human sleep differs from sleep in other primates

OBJECTIVES Primates vary in their sleep durations and, remarkably, humans sleep the least per 24-hr period of the 30 primates that have been studied. Using phylogenetic methods that quantitatively situate human phenotypes within a broader primate comparative context, we investigated the evolution of human sleep architecture, focusing on: total sleep duration, rapid eye movement (REM) sleep duration, non-rapid eye movement (NREM) sleep duration, and proportion of sleep in REM. MATERIALS AND METHODS We used two different Bayesian methods: phylogenetic prediction based on phylogenetic generalized least squares and a multistate Onrstein-Uhlenbeck (OU) evolutionary model of random drift and stabilizing selection. RESULTS Phylogenetic prediction confirmed that humans sleep less than predicted for a primate of our body mass, predation risk, brain size, foraging needs, sexual selection, and diet. These analyses further revealed that humans pack an unexpectedly higher proportion of REM sleep within a shorter overall sleep duration, and do so by reducing NREM sleep (rather than increasing REM). The OU model generally confirmed these findings, with shifts along the human lineage inferred for TST, NREM, and proportion of REM, but not for REM. DISCUSSION We propose that the risks and opportunity costs of sleep are responsible for shorter sleep durations in humans, with risks arising from terrestrial sleep involving threats from predators and conspecifics, and opportunity costs because time spent sleeping could be used for learning, creating material objects, and socializing.

Does the moon influence sleep in small-scale societies?

Objectives: The lunar cycle is expected to influence sleep‐wake patterns in human populations that have greater exposure to the environment, as might be found in forager populations that experience few environmental buffers. We investigated this “moonlight” hypothesis in two African populations: one composed of hunter‐gatherers (with minimal environmental buffering) and the other rural agriculturalists (with low‐to‐moderate environmental buffering). Setting: Research was conducted on Hadza hunter‐gatherers from the Sengele community near Lake Eyasi in northern Tanzania and in Mandena, Madagascar, in a rural community of approximately 4000 farmers. Participants: Thirty‐one adult Hadza and 21 Malagasy adults were recruited. Measurements: We used the CamNtech Motionwatch 8 actigraph and generated data on an epoch‐by‐epoch, 1‐minute basis. Results: In general support of the moonlight hypothesis, we uncovered an association between sleep‐wake patterns and lunar cycle (ie., moonlight) for Hadza hunter‐gatherers. However, the direction of the effect was opposite to what we predicted: as the potential for exposure to moonlight increased, activity generally shifted to a pattern of less nighttime activity and greater daytime activity. No significant effects were found in the Malagasy agriculturalists. Conclusions: The proposal that human behaviors are linked with moon phase is a popular belief that persists despite the absence of consistent evidence. We provide the first direct evidence that lunar cycle is linked to sleep‐wake pattern in a hunter‐gatherer society, suggesting that moonlight does not inhibit sleep‐wake patterns in the ways that electric lighting does.