The expensive-tissue hypothesis proposes that brain enlargement during human evolution was offset by a reduced gut size. The finding that the typical trade-off in mammals is between brain size and fat reserves suggests otherwise. See Letter p.91
Brain enlargement is one of the more conspicuous aspects of human evolutionary history. Although the benefits of a large brain seem obvious, the correlated survival and metabolic costs are immense and define much about the human condition. In Homo sapiens, giving birth to big-brained babies is risky. Furthermore, the energy consumed by the brain forms roughly 65% of a baby's total consumption and no less than 20–25% of an adult's, even though brain tissue accounts for only 2% of adult body mass.
An enduring question, then, is how the energetic costs of evolving a larger brain were overcome, eventually enabling a threefold increase in volume in the transition from the hominin Australopithecus to H. sapiens (Fig. 1). On page 91 of this issue, Navarrete et al.1 address this problem by presenting an impressive data set comparing mammalian brain size with the mass of visceral organs and fat deposits. Their results challenge the compelling idea that brain enlargement in Homo and other mammals can be 'financed' by a reduction in gut size.
The idea contested by Navarrete et al. is known as the expensive-tissue hypothesis2. It argues that the gastrointestinal tract is the only energetically costly organ system in humans and other primates that correlates negatively with brain size. Furthermore, a reduced gut is characteristic of primates that have high-quality diets. Because access to substantial quantities of meat and other new food resources has improved the quality of the diet of ancestral humans over the past 2.5 million years, this is expected to have allowed the human gut to become smaller. A key part of the expensive-tissue hypothesis, therefore, is that the costs of brain expansion in Homo were covered by this reduction in gut size.
According to the opposing view now offered by Navarrete et al., the gut–brain trade-off should be replaced by a fat–brain trade-off. The authors took on the ambitious task of dissecting and measuring fat tissue mass in 100 species of mammals. They discovered that brain size correlates negatively with the amount of body fat in most mammals, but not with the mass of the gut, liver or any other tissue that has been proposed to be energetically expensive in mammals.
The lack of a negative relationship between expensive tissues and brain size across many mammalian groups led the authors to dispute the idea that human brain enlargement was paid for by energy savings associated with a reduced gastrointestinal tract. Instead, they suggest that increasing body fat and brain size are complementary strategies for warding off starvation. In other words, an organism's capacity to store body fat, which is a relatively inexpensive way to buffer food scarcity, can be reduced in lineages in which a bigger brain allows better-quality food intake or lowers the energetic costs of other life functions.
But what about primates? And how does this finding1 help to explain the particular case of H. sapiens? Navarrete et al. did not observe a reciprocal relationship between brain size and fat reserves in primate species. They attribute this result to the fact that the primates they studied were captive animals — and thus not truly representative of primates in their natural environment — and to the diverse ways in which primates store fat, among other factors. As for H. sapiens, our species is unusual in having not only a large brain, but also hefty fat deposits — a dual strategy for combating starvation that was apparently beneficial in the variable and unpredictable habitats in which Homo evolved. Whereas most mammalian species employ one or the other strategy, the evolution of both in Homo, according to Navarrete et al., depended on the evolution of energetically efficient bipedal locomotion. Lowering the energy costs of locomotion early on in evolution might have allowed humans to evolve fat-storage capacity along with an expensive brain.
The authors' study1 admirably draws attention to several other factors relevant to brain expansion in Homo. The use of tools, cooking and advances in foraging technologies, for example, would have improved the food supply for Homo and so stabilized energy intake. Brain expansion was also helped by the development of behaviour such as giving resources to other individuals — a peculiar dimension of human social interactions that comes with expectations that adults will share and eat food together and cooperate in caring for the young. Such behaviour might have reduced the amount of energy expended by reproductive females and dependent offspring, thereby allowing an increase in brain size and birth rate, along with a slower pace of development for infants.
When considering the above suggestions, one is confronted by the unique outcomes of human evolution. It is good science to seek biological explanations for specific evolutionary features by using principles that are applicable across the widest range of species. Biological principles have, however, led to uncommon outcomes in humans. Compared with other mammals, human carers make an enormous investment in offspring, and they require atypically cooperative efforts to meet the time and energy demands of an infant's prolonged maturation. A keen acquisitiveness of energy-rich resources is another defining human quality, as this is imperative for feeding our hungry brain. These and other remarkable outcomes of general evolutionary processes have led to proposed explanations for the explosion in human brain size — including the expensive-tissue hypothesis — that fall 'outside the box' of general mammalian rules. Such explanations are arguably not ideal, but are acceptable as long as they are based on solid empirical data and comparative biological reasoning.
Navarrete and colleagues, however, pursue an explanation that applies generally across mammals — an approach that is both refreshing and provocative. Inevitably, some will ask: could it be that gut-size reduction helped pay for brain enlargement in our genus, even if it did not do so in most other mammals? It is impossible to rule this out, but the authors' hypothesis1 does neatly tie together many facets of human evolutionary history, without invoking a gut–brain trade-off. Fat now looms large in explanations of human evolution, and will probably feed debates for years to come.
Navarrete, A., van Schaik, C. P. & Isler, K. Nature 480, 91–93 (2011).
Aiello, L. C. & Wheeler, P. Curr. Anthropol. 36, 199–221 (1995).
Holloway, R. L., Broadfield, D. C. & Yuan, M. S. The Human Fossil Record Vol. 3 (Wiley, 2004).
Falk, D. et al. Proc. Natl Acad. Sci. USA 104, 2513–2518 (2007).
Carlson, K. J. et al. Science 333, 1402–1407 (2011).
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