The new evidence regarding how the brain creates smell and flavor that dominate our daily lives suggests the hypothesis that the human brain flavor system may have played a much larger role in human evolution than is appreciated. There has been little discussion of this possibility up to now. Speculations on how evolution occurred are notoriously difficult to make. However, in pursuing this question I have been greatly encouraged by interactions with anthropologists. It will be useful to identify some of the evidence for events in human evolution in which the human brain flavor system may have played a significant role. Five kinds of evidence seem most interesting: (1) the record of the genes; (2) competition between smell and sight; (3) the increase in brain size; (4) the adaptations of the musculoskeletal system for searching for food; and (5) the control of fire and the development of human cuisines.
The Record of the Genes
We have seen that the olfactory receptor genes are believed to be the largest family in the mammalian genome, accounting for 2 to 5 percent of the total, depending on one’s estimate of the total number of genes. The large gene families were likely also characteristic of the ancient ancestors; dynamic changes presumably occurred constantly over time but the approximate sizes of the families were maintained because of their adaptive value.
Mammalian and primate evolution accelerated with the extinction of the dinosaurs around 65 million years ago. The original large size of the mammalian receptor family was more or less maintained as mammals diverged into their different orders, families, and species, as attested to by the large repertoire present in most mammals today. It is also likely that, as in modern mammals, the receptor cells projected to the glomerular sheet in the olfactory bulb, where spatial patterns were elicited by the different odors as we discussed in chapter 7. This assumption is strongly supported by the fact that glomeruli are a phylogenetic constant for the processing of smell across almost all vertebrates as well as invertebrates, as John Hildebrand and I reviewed in 1997. The olfactory system thus provides a backward reach into evolutionary time. It may be unique among brain systems for this purpose because of the close relation between the receptor genes and the images of the odor world that they form in the brain.
What was happening to the mammalian smell receptor repertoire during the evolution of modern primates, including humans? The genes for several species were sequenced and compared by Sylvie Rouquier and her colleagues in 2000. When arranged in order of branching from the primate tree, it appears that the number of functional genes has undergone a steady decline, from almost 100 percent in lemurs through the modern species of howler, macaque, baboon, chimp, to humans at about 35 percent. On the surface, this would seem to confirm the decline of the importance of smell in humans as opposed to most other mammals. However, we’ve seen that this conclusion has been challenged by Matthias Laska and his colleagues, then in Munich, who from testing monkeys and comparing with humans has provided evidence that primate olfaction is quite good compared with rodents and even dogs. Furthermore, in chapter 9 we saw that the number of receptors has to be evaluated within the context of the number of receptor cells and the number of olfactory glomeruli; the correlations appear to be complex. In addition, a major thesis of this book is that the declining numbers of olfactory receptor genes during human evolution are offset by brain size, as the forebrain expanded vigorously, and the olfactory pathway still had its privileged direct access. There were thus two balancing trends, a gradual reduction in the peripheral smell sensory receptor repertoire, offset by a large expansion of the central brain systems for analyzing the images. The expansion associated with consumption of more flavorful foods enhanced the system that created the flavors.
Competition Between Smell and Sight
The first primates of modern aspect appeared about 60 million years ago. These animals have dental and anatomical adaptations that indicate omnivory was a typical and successful primate adaptation. Their skeletal features suggest increases in manipulative abilities, a variety of locomotor patterns, and a reliance on vision. Because of forward-facing orbits and reduced snouts, lists of early primate features usually include reduced reliance on the olfactory sense. It is believed that the forward movement of the eyes required a reduction of the snout and, with it, a reduction in the size of the olfactory sensory receptor population and therefore in the smell part of the brain. This presumed decline of smell in the evolution of primates is one of the most entrenched ideas in anthropology and in the public mind.
The new evidence regarding the brain flavor system indicates that this idea needs to be revised. An increase in visual acuity does not necessarily mean reduced olfactory sensitivity and discrimination. A major new theme is that a smaller olfactory receptor repertoire in primates is offset by the larger brain size and the more complex processing of the smell signals. This reassessment is supported by behavioral studies that indicate that monkeys and humans have senses of smell that are quite good.
Like other mammals, therefore, primates likely were dominated by their sense of smell. The ripeness of fruit can be determined by feel or by sight, but perhaps most effectively by scent. Fruit eating in the jungle also required a more complex lifestyle: remembering when fruit is likely to ripen, making the necessary plans to be there at the right time, feeding the infants, and sharing among the members of the clan. More complex brains, dominated by an expanding neocortex, gave a competitive advantage in organizing these activities. In addition, like modern primates they likely used scent to identify individuals and to determine the social standing of particular animals.
Life among the trees thus required smell and larger brains and also required an excellent sense of vision. Most primates therefore have large eyes to enable both day and night vision. Many species also benefit from excellent color vision, using color to aid, for example, in judging the ripeness of fruit. High-acuity eyesight was also useful in plucking the fruit and bringing it close to the face for examining it visually for ripeness. In our view from the perspective of the nose, thus began one of the driving forces in primate evolution: the competition between smell and sight for control of the neocortex in primate behavior.
Increasing Brain Size
The earliest humans branched off from the lines leading to modern-day African apes about 5 to 6 million years ago. At that time, climate changes were causing a decrease in rainfall and the coming of different seasons. The environment changed, too. In Africa, the dense forests with their profusion of plant life and fruit trees were giving way to stands of trees scattered over grasslands and semideserts. It is hypothesized that in such a landscape, bipedalism gave early hominids an adaptive advantage in their search to find the increasingly scattered sources of food. Because these creatures were omnivorous, their diet probably included leafy greens, flowers, nuts, small vertebrates, insects, and fruits. One could imagine that because of their high sugar content, fruits were preferred food items for our hominid ancestors. As Rick Potts has noted, “The ephemeral aspect of high-quality fruit has placed a premium on cognitive and social means of finding and defending food sources.” These cognitive and social demands are regarded as critical elements in the evolution of the primate brain leading to humans. From the present perspective, the importance of smell and flavor could be recognized in motivating the search, guiding it to its target fruit, discerning ripeness, and finding gratification in the consumption. In this view, it was not diet per se that was the initiating factor underlying the expansion of the primate brain, but the search for flavor. From the perspective of neuro-economics (chapter 22), flavor put values on the food in the diet.
In the consensus view, early bipedal hominids were able to hunt more successfully for food, mainly fruit. In our view through the nose, they were motivated to find it by its smell, they judged its ripeness mainly by its smell, and they obtained pleasure and reward from eating it by its smell and flavor.
Achieving bipedalism required a number of delicate adjustments to the musculoskeletal system. It is tempting to suggest that many of them also served to acquire flavorful foods. Adaptations of the pelvis enabled a hominid to squat while grasping food with its hands, manipulating it, smelling it, and eating it. Keen eyesight enabled it to examine the food closely. An enlarging neocortex provided fine motor control of the fingers, which, together with high-acuity eyesight, enabled the hominid to search for other food sources. Adaptations of the motor pathways of the brain brought cortical control of each separate finger, so that individual seeds on the ground could be picked up and eaten. This fine control of the fingers occurred through direct connections from the motor nerve cells in the neocortex to the motor neurons in the spinal cord that innervate the finger muscles. A sharp sense of smell enabled these creatures not only to test every food by sniffing it but also to sense the flavors of ingested foods. Because the early hominids were omnivores, the foods consisted of novel mixtures, giving rise to new flavors from combinations of fruits, seeds, leaves, and small animals. It was the first step toward cuisine.
Around 2 million years ago a distinctly new type of hominid (Homo ergaster or Homo erectus) emerged, distinguished by a larger, more habitually upright body and a larger brain, both in absolute terms and relative to body size. It is assumed that these anatomical changes reflect a significant dietary change, including plenty of fat for the myelin that would have been needed in the larger brain. The diet of these humans, like that of modern-day humans, remained that of an omnivore, containing fruits and vegetables, roots, insects, and honey in addition to meat and marrow. It may be hypothesized that the flavors were learned to be advantageous for health, although the connection between flavor and nutrition remains one of the most challenging problems in research on feeding behavior.
Musculoskeletal Adaptations for Acquiring Flavorful Food
According to the current consensus, about 2 million years ago some humans migrated out of Africa, and some reached as far as Indonesia in a very short (evolutionarily speaking) period of time. This may have been facilitated by not only the larger upright stature and larger brains, but also the skeletal changes that appear to reflect adaptations for long-distance walking and running. What does this have to do with smell?
Among my anthropologist colleagues, Daniel Lieberman has shared much of my enthusiasm for rethinking the role of flavor in human evolution. We have seen that he has carried out deep studies of the evolution of the human head, providing new insights into the structural changes that would have contributed to retronasal smell. The adaptations of the head and body for long-distance running have been another area of interest. Dennis Bramble and Lieberman, in an article published in 2004, list 26 derived features of the skeleton that would have aided long-distance running, such as longer leg bones (for longer strides), wider joint cartilages (to absorb jolts), and more flexible relations between torso and limbs to allow better balance while running. These adaptations thus must be added to those for reaching, squatting, and examining food items that we have mentioned previously. It is striking that a short snout is listed as an adaptation for running and walking by making the head more balanced and thus aiding in head stabilization. This is a good example of how one has to take a broad behavioral perspective on the basis for biological adaptations. These and other adaptations are explained in full in Lieberman’s book The Evolution of the Human Head.
What induced these early humans to journey thousands of miles over the Asian continent to China and Southeast Asia? Some cite wanderlust, a human curiosity to explore. But could these humans have been motivated to find new sources of foods? From the nose’s perspective, a new possibility is the motivation to find plants that added flavors to the diet, the ancestral equivalents of herbs and spices. Later waves of human migrations over the spice trade routes during recorded history were driven by this craving for flavors. As we have seen, the craving center is a central component of the human flavor system, and smell is the main input.
Fire, Flavor, and Cuisine
A critical event was the use of cooking for preparing foods. When it began, and what has been its significance, has been controversial. The earliest statement I have found is from the late eighteenth century by James Boswell, best known as the biographer of Samuel Johnson, but also a devoted gourmand:
Dr. [Benjamin] Franklin said, Man was a ‘tool-making animal,’ which is very well; for no animal but man makes a thing, by means of which he can make another thing. But this applies to very few of the species. My definition of Man is, a ‘Cooking Animal.’ The beasts have memory, judgement, and all the faculties and passions of our mind, in a certain degree; but no beast is a cook.
In recent decades, many authors from many fields—anthropology, history, cooking, archaeology, sociology—have echoed this claim: “[C]ooking establishes the difference between animals and people” (Claude Lévi-Strauss); cooking defines “the human essence” (Michael Symons); cooking is an “index of the humanity of humankind” (Felipe Fernández-Armesto). But Richard Wrangham, from whose book Catching Fire: How Cooking Made Us Human these quotations are taken, points out that these claims are that “cooking had shaped us, but they did not say why or when or how.”
To answer those questions, Wrangham has drawn on several decades of fieldwork and research to identify what fire actually would have done to influence the evolution of early humans. For this, he has essentially carried out the kind of analysis of what fire does to make meat and vegetables more easily chewed and flavorful, in parallel with the similar analyses that current food critics and chefs are carrying out on modern cuisines under the banner of molecular gastronomy and other movements. This has allowed him to focus on the key contribution that cooking made: the increased amount of energy, and the rapidity with which it could be acquired, from cooked foods. He provides evidence that the use of controlled fire for this purpose was contemporaneous with the spurt in brain size that characterized the passage from Homo erectus to Homo sapiens. This would mean that fire was controlled more than a million years before the best evidence for it has been found, but his arguments are persuasive.
I met Wrangham almost a de cade ago, after I contacted him to discuss the early evidence for odor images and retronasal smell. He kindly invited me to give a seminar to the Department of Anthropology at Harvard, hich stimulated a lively discussion and gave me encouragement toward developing the human brain flavor system hypothesis that adds to his hypothesis by making more explicit the brain mechanisms involved.
Cooking is important culturally because of the complex social organization that arises around it. Some individuals provide meat, others gather vegetables and other food items; there must be people who store it and guard it; the food must be prepared; preparation requires receptacles, whether in the ground or made into bowls and pots; there must be tools fashioned into utensils to cut and stir; and the family or local group must organize itself for consuming the food together around the cooking site. There is general agreement, as indicated in the earlier quotations, and as expounded many years ago by Peter Farb and George Armelagos in their book Consuming Passions: The Anthropology of Eating, that cooking was the activity that more than any other formed human society. Our new perspective extends that view: flavor was the glue that bonded societies together around the shared prepared meal.
To organize all these activities, exchange of information was essential. Some kind of language must have emerged to knit these complex emerging societies together. Steven Pinker in The Language Instinct: How the Mind Creates Language suggests that language arose in humans well before anatomically modern humans populated the Old World 40,000 years ago. Although there is no direct evidence for the first use of language, we may hypothesize that it arose in close association with the emergence of the divisions of labor and complex social interactions we have noted that are related to cooking. The more complex those relations became, the more extensive the vocabulary and complex the grammar.
This is where smell again comes into the picture. Although it is rarely mentioned in traditional accounts of the diets of our ancestors, the sensory qualities were likely to have been one of the main topics of conversation around the campfire as the food preparations proceeded and as the food was tasted and consumed. This would apply to the aroma before eating and even more to the flavor of the ingested food, which as we have noted is mostly due to smell. This ties smell, flavor, and language together in a way seldom recognized: the smells and flavors of cooking were likely a prime factor in the development of language. At first this seems counterintuitive because of the common belief that it is difficult to describe smells in words. But if smells and flavors are patterns that the brain creates, as we have shown, the patterns are part of the reason smells and flavors played the role they did.
In conclusion, the idea that the sense of smell has been reduced in the course of human evolution is one of the most entrenched ideas in anthropology and in the public mind. A broad range of research indicates that it is time to revise this view and incorporate odor images, the perception of flavor, and the extensive brain mechanisms they engage into an enlarged and enriched understanding of the biological basis of human behavior.