The high energetic costs of human brain development have been hypothesized to explain distinctive human traits, including exceptionally slow and protracted preadult growth. Although widely assumed to constrain life-history evolution, the metabolic requirements of the growing human brain are unknown. We combined previously collected PET and MRI data to calculate the human brain's glucose use from birth to adulthood, which we compare with body growth rate. We evaluate the strength of brain-body metabolic trade-offs using the ratios of brain glucose uptake to the body's resting metabolic rate (RMR) and daily energy requirements (DER) expressed in glucose-gram equivalents (glucose rmr% and glucose der% ). We find that glucose rmr% and glucose der% do not peak at birth (52.5% and 59.8% of RMR, or 35.4% and 38.7% of DER, for males and females, respectively), when relative brain size is largest, but rather in childhood (66.3% and 65.0% of RMR and 43.3% and 43.8% of DER). Body-weight growth (dw/dt) and both glucose rmr% and glucose der% are strongly, inversely related: soon after birth, increases in brain glucose demand are accompanied by proportionate decreases in dw/dt. Ages of peak brain glucose demand and lowest dw/dt co-occur and subsequent developmental declines in brain metabolism are matched by proportionate increases in dw/dt until puberty. The finding that human brain glucose demands peak during childhood, and evidence that brain metabolism and body growth rate covary inversely across development, support the hypothesis that the high costs of human brain development require compensatory slowing of body growth rate.neuroimaging | diabetes | human evolution | neuronal plasticity | anthropology A prolonged period of childhood and juvenile growth is a defining feature of human life history (1-3). Compared with other great apes, human offspring are weaned early, leading to an extended period of dependence on procured resources rather than breast milk (1, 4). Although this unique human reproductive pattern is viewed as shortening the interbirth interval and thus increasing fertility (5, 6), what is less clear is why humans also grow so slowly during childhood. Although most primates grow slower than other mammals (7), human childhood and juvenile growth stand out as unusually slow even by primate and great ape standards, during which it proceeds at a pace more typical of reptiles than of mammals (8, 9). In humans, a sizeable percentage of preadult growth is deferred until the pubertal growth spurt, when growth rate markedly increases and adult size is achieved (1).Many hypotheses have been proposed to explain this slow and prolonged preadult life-stage, with most pointing to the extra time and energy required for human learning and brain development (5, 10-12). It has long been assumed that human cultural practices are sufficiently complex that they take many years to learn, which could have selected for a slowing down and extension of preadult development (13). A recent variant of this idea notes the importance of ...
Although it has been believed that brown adipose tissue (BAT) depots disappear shortly after the perinatal period in humans, PET imaging using the glucose analog 18F-FDG has shown unequivocally the existence of functional BAT in adult humans, suggesting that many humans retain some functional BAT past infancy. The objective of this study was to determine to what extent BAT thermogenesis is activated in adults during cold stress and to establish the relationship between BAT oxidative metabolism and 18F-FDG tracer uptake. Methods Twenty-five healthy adults (15 women and 10 men; mean age ± SD, 30 ± 7 y) underwent triple-oxygen scans (H215O, C15O, and 15O2) as well as measurements of daily energy expenditure (DEE; kcal/d) both at rest and after exposure to mild cold (15.5°C [60°F]) using indirect calorimetry. The subjects were divided into 2 groups (high BAT and low BAT) based on the presence or absence of 18F-FDG tracer uptake (standardized uptake value [SUV] > 2) in cervical–supraclavicular BAT. Blood flow and oxygen extraction fraction (OEF) were calculated from dynamic PET scans at the location of BAT, muscle, and white adipose tissue. Regional blood oxygen saturation was determined by near-infrared spectroscopy. The total energy expenditure during rest and mild cold stress was measured by indirect calorimetry. Tissue-level metabolic rate of oxygen (MRO2) in BAT was determined and used to calculate the contribution of activated BAT to DEE. Results The mass of activated BAT was 59.1 ± 17.5 g (range, 32–85 g) in the high-BAT group (8 women and 1 man; mean age, 29.6 ± 5.5 y) and 2.2 ± 3.6 g (range, 0–9.3 g) in the low-BAT group (9 men and 7 women; mean age, 31.4 ± 10 y). Corresponding maximal SUVs were significantly higher in the high-BAT group than in the low-BAT group (10.7 ± 3.9 vs. 2.1 ± 0.7, P = 0.01). Blood flow values were significantly higher in the high-BAT group than in the low-BAT group for BAT (12.9 ± 4.1 vs. 5.9 ± 2.2 mL/100 g/min, P = 0.03) and white adipose tissue (7.2 ± 3.4 vs. 5.7 ± 2.3 mL/100 g/min, P = 0.03) but were similar for muscle (4.4 ± 1.9 vs. 3.9 ± 1.7 mL/100 g/min). Moreover, OEF in BAT was similar in the 2 groups (0.51 ± 0.17 in high-BAT group vs. 0.47 ± 0.18 in low-BAT group, P = 0.39). During mild cold stress, calculated MRO2 values in BAT increased from 0.97 ± 0.53 to 1.42 ± 0.68 mL/100 g/min (P = 0.04) in the high-BAT group and were significantly higher than those determined in the low-BAT group (0.40 ± 0.28 vs. 0.51 ± 0.23, P = 0.67). The increase in DEE associated with BAT oxidative metabolism was highly variable in the high-BAT group, with an average of 3.2 ± 2.4 kcal/d (range, 1.9–4.6 kcal/d) at rest, and increased to 6.3 ± 3.5 kcal/d (range, 4.0–9.9 kcal/d) during exposure to mild cold. Although BAT accounted for only a small fraction of the cold-induced increase in DEE, such increases were not observed in subjects lacking BAT. Conclusion Mild cold-induced thermogenesis in BAT accounts for 15–25 kcal/d in subjects with relatively large BAT depots. Thus, although the presen...
This study reevaluates the long-standing observation that human morphology varies with climate. Data on body mass, the body mass index [BMI; mass (kg)/stature (m)2], the surface area/body mass ratio, and relative sitting height (RSH; sitting height/stature) were obtained for 223 male samples and 195 female samples derived from studies published since D.F. Roberts' landmark paper "Body weight, race, and climate" in 1953 (Am. J. Phys. Anthropol. 11:533-558). Current analyses indicate that body mass varies inversely with mean annual temperature in males (r=-0.27, P < 0.001) and females (r=-0.28, P < 0.001), as does the BMI (males: r=-0.22, P=0.001; females: r=-0.30, P < 0.001). The surface area/body mass ratio is positively correlated with temperature in both sexes (males: r=0.29, P < 0.001; females: r=0.34, P < 0.001), whereas the relationship between RSH and temperature is negative (males: r=-0.37, P < 0.001; females: r=-0.46, P < 0.001). These results are consistent with previous work showing that humans follow the ecological rules of Bergmann and Allen. However, the slope of the best-fit regressions between measures of body mass (i.e., mass, BMI, and surface area/mass) and temperature are more modest than those presented by Roberts. These differences appear to be attributable to secular trends in mass, particularly among tropical populations. Body mass and the BMI have increased over the last 40 years, whereas the surface area/body mass ratio has decreased. These findings indicate that, although climatic factors continue to be significant correlates of world-wide variation in human body size and morphology, differential changes in nutrition among tropical, developing world populations have moderated their influence.
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There is currently great interest in developing ecological models for investigating human evolution. Yet little attention has been given to energetics, one of the cornerstones of modern ecosystem ecology. This paper examines the ecological correlates of variation in metabolic requirements among extant primate species, and uses this information to draw inferences about the changes in energy demands over the course of human evolution. Data on body size, resting metabolism, and activity budgets for selected anthropoid species and human hunter-gatherers are used to estimate total energy expenditure (TEE). Analyses indicate that relative energy expenditure levels and day ranges are positively correlated with diet quality; that is, more active species tend to consume more energy-rich diets. Human foragers fall at the positive extremes for modern primates in having high expenditure levels, large ranges, and very high quality diets. During hominid evolution, it appears that TEE increased substantially with the emergence of Homo erectus. This increase is partly attributable to larger body size as well as likely increases in day range and activity level. Assuming similar activity budgets for all early hominid species, estimated TEE for H. erectus is 40-45% greater than for the australopithecines. If, however, it is assumed that the evolution of early Homo was also associated with a shift to a more "human-like" foraging strategy, estimated expenditure levels for H. erectus are 80-85% greater than in the australopithecines. Changing patterns of resource distribution associated with the expansion of African savannas between 2.5 and 1.5 mya may been the impetus for a shift in foraging behavior among early members of the genus Homo. Such ecological changes likely would have made animal foods a more attractive resource. Moreover, greater use of animal foods and the resulting higher quality diet would have been important for supporting the larger day ranges and greater energy requirements that appear to have been associated with the evolution of a human-like hunting and gathering strategy.
Total daily energy expenditure (“total expenditure”) reflects daily energy needs and is a critical variable in human health and physiology, but its trajectory over the life course is poorly studied. We analyzed a large, diverse database of total expenditure measured by the doubly labeled water method for males and females aged 8 days to 95 years. Total expenditure increased with fat-free mass in a power-law manner, with four distinct life stages. Fat-free mass–adjusted expenditure accelerates rapidly in neonates to ~50% above adult values at ~1 year; declines slowly to adult levels by ~20 years; remains stable in adulthood (20 to 60 years), even during pregnancy; then declines in older adults. These changes shed light on human development and aging and should help shape nutrition and health strategies across the life span.
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