Ann Gibbons
Science 1998; 280: 1345-1347.
To understand brain evolution, anthropologists and neuroscientists are analyzing the energetic constraints on brain size--and how humans may have evolved a way around them
Humans have voracious brains. A newborn's brain consumes 60% of the energy the baby takes in. And that's just the beginning. That lump of gray matter doubles in size in the first year of life, and by adulthood, human brains weigh roughly a kilogram more than the brains of similar-sized mammals. Many researchers think energy intake limits brain size in many mammals. Yet the human brain and body as a whole don't use any more energy than smaller brained mammals of similar body size, so something must be making up for the brain's outsized appetite. As Leslie C. Aiello, a paleoanthropologist at University College London, puts it: "Where does the energy come from to fuel the large brain?" And if there is an energetic constraint on how big a brain can get, how did our ancestors overcome that limit?
Last month at the annual meeting of the American Association of Physical Anthropologists (AAPA), anthropologists debated two solutions to the brain's energy crisis: One, called the expensive tissue hypothesis, is that big brains in adults are fueled by the energy saved in humans' relatively small gastrointestinal (G.I.) tracts, which we can afford because of our high-quality diet. The other idea, the maternal investment hypothesis, proposes that most of the extra energy comes early in life--from mom, through the placenta during pregnancy and through breast milk between birth and age 4, when the human brain reaches 85% of its adult size.
At the moment, as researchers test and amplify each theory, it's unclear if either one is right; it may be that both play a role at different times in development. Either way, a growing number of anthropologists and neuroscientists are analyzing the potential constraints on brain evolution, testing their ideas with data from genetics, neuroscience, and comparative physiology. "The notion of understanding brain change in terms of the constraints on the body is an interesting and novel way of coming at this problem," says Cornell University neuroscientist Barbara Finlay.
Most evolutionary theories focus on the environmental or social factors that might have favored big brains, but this approach analyzes another variable: the underlying physical constraints that had to be overcome to build an oversized brain. By putting the two together, researchers hope to come up with more realistic evolutionary scenarios of how changes in our ancestors' behavior or ecology, such as hunting and living in large groups, helped them evolve bigger brains. Says paleoanthropologist Dean Falk of the State University of New York, Albany: "I'm really all for this approach. We have to attend to the energetics or we're not going to get selection for a bigger brain going on at all."
Researchers have long known that an animal's body size is a critical influence on brain size, as shown at the turn of the century by renowned Dutch paleontologist Eugene Dubois. Brains consume large quantities of energy in making neurotransmitters and firing axons, and bigger bodies have bigger hearts and lungs to supply more energy and oxygen to the brain. That's why elephants and baleen whales can have brains four to six times larger than those of humans. But humans are different. Our brains have tripled in size since Lucy and her fellow australopithecines, with brains roughly the size of a chimpanzee, began to walk upright on the African savanna 3 million years ago. But our bodies aren't even twice as big. "Humans, in fact, have the largest brain size relative to body size among placental mammals," says University of Zurich primatologist Robert D. Martin.
Nor do humans conform to another pattern that Martin noticed in the early 1980s when he was pondering the question of human brain size. Research on basal metabolic rates, or how much energy an animal consumes while resting, showed that in mammals, the size of the newborn's brain tends to correlate with the mother's metabolic rate. Martin and others reasoned that supporting a bigger brain requires a higher energy consumption. Yet humans' basal metabolic rate is no higher than that of large sheep, which have brains five times smaller. Humans are apparently getting enough energy to feed their brains without increasing their overall energy intake, so it must be coming from some other source.
That source is the gut, according to the expensive tissue hypothesis, first proposed in 1995 by Aiello and physiologist Peter Wheeler of Liverpool John Moores University and revised last month by Aiello at the AAPA. The pair reviewed studies of humans and found that most of the basal metabolic rate--more than 70%--goes to fuel the brain, heart, kidney, liver, and G.I. tract. To find out if the demands of any of these organs were reduced to fuel the human brain, they compared the mass of each organ in adult humans with that expected for a primate of similar body size. Only the G.I. tract was smaller than expected--and it was about 60% of the size expected for a similar-sized primate. "The increase in mass and energy consumption of the human brain appears to be balanced by an almost identical reduction in the size of the gastrointestinal tract," concludes Aiello.
Aiello speculates that we could reduce our gut size to free up energy for a larger brain because of a dietary change that was taking place as brain size expanded. Our ancestors were shifting from a heavily vegetarian diet, which requires a massive gut to digest plants and nuts, to a more easily digestible, nutritious diet that included meat and requires less gut tissue.
Other researchers are now testing Aiello's idea. Harvard University primatologist Richard Wrangham and his students compared pigs--animals "rumored to be quite smart," says Wrangham--with mammals such as cattle, sheep, goats, and deer. Pigs have small stomachs compared with these mammals, but their brains are no larger, showing that the gut-brain trade-off didn't apply to them. Other studies have shown that the theory doesn't hold for birds or bats. In fact, it may apply only to some primates. But Aiello and Wrangham aren't bothered by this. "Other animals, such as birds, have different energetic challenges," says Aiello. Birds, for example, put their energy into large hearts for flight and have small guts and brains. "I'm not worried about it," agrees Wrangham. "I think Aiello and Wheeler have got the right answer."
But Martin thinks another source of energy may be more important in building and fueling big brains: energy donated by the mother. He thinks the obvious place to look for extra energy in humans is during the "crunch time" for brain development--from gestation until age 4, when the brain reaches 85% of its full adult size. That trail led straight to the mother, who "provides most of the energy in gestation, then in lactation, which is 3 to 4 years in hunter-gatherers," says Martin.
Indeed, work by other researchers makes it clear that during gestation at least, the human system has evolved to allow maximum energy transfer between mother and offspring. The human placenta is particularly greedy, sucking nutrients from the mother's bloodstream more aggressively than in other primates, according to recent work by Harvard University evolutionary biologist David Haig. He notes that in humans the placenta invades the uterine lining more deeply than in other primates. This energy drain continues in lactation. Human gestation is over well before brain growth is complete, in contrast to other animals. Lactation takes up the slack, says Martin. In effect, human gestation continues in the first year of life. "We achieve our big brains in continuing our fetal pattern of growth in the first year of life, and human milk must be pumping in energy," says Martin. Thus humans can afford such big brains because their mothers make such an enormous investment in them, nursing them until brain growth is almost complete.
The only way human mothers can donate so much energy to brain growth in their infants is by taking in extra energy themselves. Paleoanthropologist Alan Walker of Pennsylvania State University, University Park, has an as-yet-unpublished proposal about how human ancestors met this need. Like Aiello, he thinks the switch to a diet high in protein and fat 2 million years ago, with the advent of hunting, was crucial. In his scenario, however, the new diet's role in brain evolution allowed a fetus to pull this much energy from the mother without killing her.
Social changes may have played a role, too. As our species evolved, mothers could increasingly count on family members to feed them and to help care for their young, so they could invest more in pregnancies and infants, says Cambridge University behavioral neuroscientist Eric Keverne. "Mothers were getting access to more and more energy, through tool use, cooking, eating meat," says Martin. "It's progressive." So in a positive feedback loop, a higher energy intake allowed larger brains--which in turn led to even more energy intake.
So where do humans muster the energy to fuel their brainpower--mom or cheap guts? Aiello suggests both may be true. Humans may tap mom's energy resources during the period of peak brain growth in gestation and early childhood. Once weaned, small guts in later childhood and adulthood would free up energy to help sustain the expensive brain.
Despite the enthusiasm for this approach, other researchers have offered a basic challenge to the assumption behind both ideas. Although huge quantities of energy go into a working brain, energy may not be the key limiting factor in brain size, says Oxford University evolutionary biologist Paul Harvey: "There's no reason to suspect that the reason other mammals don't have big brains is that they are energetically limited."
He challenges the data that led to the assumption of an energy limit on brain growth: the link between metabolism and brain size. He and Oxford colleague Mark Pagel showed in 1988 in the journal Evolution that animals with high basal metabolic rates for their body size, such as shrews, do not produce large-brained young. "I don't see this as an energetics problem," says Harvey, whose work with Pagel suggests that the way to grow larger brains is to have long gestation times, late weaning, and fewer offspring per litter.
Others aren't ready to give up on the correlation. Martin, responding in a talk at the AAPA, says that if one incorporates length of gestation and lactation and animals' degree of independence at birth, the link between metabolism and brain size holds up.
Despite the critics, the energetic approach is making its mark, as researchers accept the possibility of energetic constraints on evolution. This "is making us do experiments to measure how much energy the mother is putting into her offspring," says Francisco Aboitiz, a neuroscientist at the University of Chile in Santiago; he is comparing brain growth in different species of rats to see how different parts of the brain have evolved in response to varying ecological conditions. In the end, both hypotheses may be pieces in a complex puzzle--important physiological constraints that had to be overcome before selection could sculpt a larger brain. "I'm sure there's no single answer," says Aiello: "These things all work together. It all depends on your ecology." And perhaps on the size of your gut or the amount of your mother's energy.