Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution

Abstract

Despite a general trend for larger mammals to have larger brains, humans are the primates with the largest brain and number of neurons, but not the largest body mass. Why are great apes, the largest primates, not also those endowed with the largest brains? Recently, we showed that the energetic cost of the brain is a linear function of its numbers of neurons. Here we show that metabolic limitations that result from the number of hours available for feeding and the low caloric yield of raw foods impose a tradeoff between body size and number of brain neurons, which explains the small brain size of great apes compared with their large body size. This limitation was probably overcome in Homo erectus with the shift to a cooked diet. Absent the requirement to spend most available hours of the day feeding, the combination of newly freed time and a large number of brain neurons affordable on a cooked diet may thus have been a major positive driving force to the rapid increased in brain size in human evolution.encephalization | expensive tissue hypothesis | brain metabolism T he human brain is a linearly scaled-up primate brain in its relationship between brain size and number of neurons (1), having evolved while being subjected to the same cellular scaling rules that apply to primates as a whole (2, 3), including great apes (4). With the largest brain among primates, humans thus have the largest number of neurons among these and possibly all mammals (5), a number that we estimate to be close to three times larger than in gorillas and orangutans, owners of the next largest brains among extant primates (4). We are not outstanding primates, on the contrary, in body size: gorillas can grow to be three times larger than humans. This discrepancy between body and brain size led to the predominant view that encephalization (that is, a larger brain size than expected for body size) is the main characteristic that sets humans apart from other primates and mammals as a whole (6). Although a relatively large brain compared with body size is expected to bring cognitive advantages (6), and despite the well-documented evidence for an increase in brain size during human evolution (7), there is still no consensus on what mechanisms or reasons led to brain enlargement in the Homo lineage.Why are the largest primates not those endowed with the largest brains as well? Rather than evidence that humans are an exception among primates, we consider this disparity to be a clue that, in primate evolution, developing a very large body and a very large brain have been mutually excluding strategies, probably because of metabolic reasons (4, 8). The brain is the third most energy-expensive organ in the human body, ranking in total organ metabolic cost below only skeletal muscle and liver (9). Accordingly, several studies have suggested that the main constraints to increasing primate brain size in evolution are metabolic in nature (10-18). The human brain, in particular, has come to cost ∼20% of the total body resting metabolic rate, even though it ...

Archaeological Starch

“…The brain accounts for 20-25% of adult basal metabolic energy expenditure [87] and red blood cells additionally require approximately 20 g glucose per day [88]. This glucose requirement is normally met from dietary carbohydrates and gluconeogenesis from non-carbohydrate sources (e.g., the glycerol moiety of triglycerides, some amino acids), or absorption of short chain fatty acids such as propionate produced in fermentations by gut microflora in the colon [89].…”

Decreasing sleep requirement with increasing numbers of neurons as a driver for bigger brains and bodies in mammalian evolution

“…I suggest that this advantage is the decrease in daily sleep requirement that ensues when the addition of neurons occurs in such a way that causes a decrease in D/A and thus a smaller rate of accumulation of metabolites underneath the surface of the parenchyma, in the self-reinforcing spiral described above. Primates, in turn, must have branched out at a point in mammalian evolution when the D/A ratio of their exclusive common ancestor was already small enough to allow only 8-9 h of sleep per day, and thus a number of daily hours of feeding that, while it later would show itself to be limiting at the upper end of body mass, still allowed a significant range of body mass and number of brain neurons [35]. Similarly, non-primate mammals appear to be born with very high neuronal densities concentrated underneath a very small cortical surface [32,36].…”

“…Increasing numbers of neurons in primate evolution does not lead to a steep enough drop in D/A to cause a significant decrease in total sleep requirement. Primates must thus sleep 8-9 h d 21 , which limits the daily number of hours spent feeding to not much more than another 8 h [35]. This is an important constraint, which we have shown to limit the maximal possible body size of primates, as well as the number of neurons that they can afford-a constraint that human ancestors escaped by radically changing their diet, possibly with cooking [35], but that still did not suffice to decrease their sleep requirement.…”

“…Primates must thus sleep 8-9 h d 21 , which limits the daily number of hours spent feeding to not much more than another 8 h [35]. This is an important constraint, which we have shown to limit the maximal possible body size of primates, as well as the number of neurons that they can afford-a constraint that human ancestors escaped by radically changing their diet, possibly with cooking [35], but that still did not suffice to decrease their sleep requirement. It will be interesting to examine whether the present hypothesis also explains the long sleep hours of species of the order Carnivora compared with artiodactyls and even primates of similar brain size [7], once data on numbers of neurons and neuronal density become available for carnivores.…”

Metabolic costs and evolutionary implications of human brain development

“…Because of its large size, the human brain has unusually high energy costs (15,20,21), which are particularly elevated compared with the body's metabolic budget early in the life cycle (18,22). It has been estimated that the human brain accounts for between 44% and 87% of resting metabolic rate (RMR) during infancy, childhood, and adolescence (23)(24)(25), suggesting strong trade-offs with other functions.…”