by John McQuaid
In the jawless fish, receptors for smell were duplicated and the extras altered to detect new scents. Their immediate ancestors likely had only a handful of smell receptors; hagfish have more than two dozen. As life evolved, this process repeated itself many times over: some animals have as many as 1,300 kinds of smell receptors; humans have more than 300.
The new sensations bombarding the first jawless fish would have been a cacophony to the brain of the average trilobite. So as the sense of smell grew sharper, the hagfish brain adapted. The olfactory bulb is a way station between the nose and the brain of all animals, converting smells to patterns of nerve impulses. In the hagfish, a new structure grew upward from the bulb, like a flower springing out of the earth. This structure was the forerunner of the cerebrum, the topmost part of the human brain that gives conscious form to virtually everything we do: it processes senses, perceptions, movement, and speech. In humans, the same sets of genes still jointly govern development of the olfactory anatomy and the brain’s basic structure. Smell has been the biological currency of feeling and action for almost as long as animals have had nostrils. It is the human sense of smell that gives flavors their vast range and subtleties. Proust, whose novel In Search of Lost Time is a reverie inspired by the scent and taste of a madeleine cookie dipped in tea, might have been taken aback to hear that carrion feeding was the starting point for humanity’s deep connection between smell and memory.
Ant Soufflé
About 250 million years ago, the global dinner table was abruptly cleared and reset. A wave of volcanic eruptions across the Siberian steppes, possibly triggered by a meteor impact, sent lava pouring over nearly a million square miles. Ash blotted out the sun for millennia. Acid rains raked the face of the planet. Plant life in the oceans and on land died off, and the atmosphere grew thick with carbon dioxide, making it all but unbreathable. This cataclysm, called the Permian extinction, eliminated 90 percent of marine species and 70 percent of land species (even most insects, which often escape such catastrophes). It was the biggest mass extinction in the history of life, a bookend to the Cambrian explosion 250 million years earlier.
Into this blighted landscape sauntered two quite different kinds of animals: dinosaurs, and creatures that looked something like small furry lizards. The outlines of this story are familiar: dinosaurs dominated the planet until their own end came, while early mammals stayed out of their way, waiting their turn. But in the shadows and hollows where mammals skulked, a different storyline was unfolding.
One of these protomammals, Morganucodon oehleri, lived about 50 million years after the Permian extinction. It wasn’t cuddly; Morganucodon laid eggs, and its long snout and ambling gait were reptilian. It had some mammalian traits: fur, warm-bloodedness, and a secondary joint in its jaw. But what really placed Morganucodon closer to the mammal camp were its heightened perceptions, forged around its endless hunt for food, which became the object of complex strategies and vivid gratification—the earliest stirrings of humans’ grand culinary passions.
Morganucodon was a wisp of a beast, shorter than a man’s finger, but its whole body responded to the world. In a single moment, it could register the scent of a tiny lizard a hundred feet away, a termite mound over the next rise, and a dinosaur across a bog. Its eyes could spy predators in the dark. It could sense animals moving nearby via slight shifts in airflow over its fur. Whiskers helped it root through the underbrush for food. It usually found what it was looking for: trails that led to anthills, worms and grubs under rotting tree trunks, tinier mammals skittering across its path. Mealtimes, which in earlier epochs were all about filling the stomach and closing the abyss of hunger, were now focused more on the delicate senses of the mouth, offering earthy flavors and hints of pleasure.
This was the world of the scavenger. If food wasn’t quickly and efficiently obtained, eaten, and digested, a Morganucodon would die, either of starvation or as some dinosaur’s snack. Mammals’ signature advance—warm-bloodedness—reflects this desperation, and the crisp urgency of each meal. Cold-blooded dinosaurs could eat and rest at varying tempos depending on how hot or cold it was, husbanding their energy. Mammals had to be constantly on the hunt, and good at it, because the metabolic furnace that maintained their body temperature demanded far more calories (a modern mammal at rest consumes seven to ten times the energy of a reptile the same size). As time went by and dinosaurs grew larger, mammals had to pour still more energy into evading them.
A new brain structure evolved to manage these challenges. In humans, the neocortex is the outer layer of gray tissue that covers the rest of the brain (cortex is Latin for “rind”). Only mammals have a neocortex, and most are smooth; only human and ape neocortices are lined with the characteristic grooves and folds that greatly increase surface area, and thus processing power. Structures in the neocortex are responsible for most of our conscious perceptions, including flavor. It’s here where feelings, urges, and impressions bubble up to awareness and spur us to act. But the early mammalian neocortex’s most important job was to be a map of lived experience, recording smells, mates, threats, and meals—what tasted good and filled the stomach, where it could be found, and the tactics that had obtained it. Flavors now made tightly woven neural patterns of sensation, memory, and behavioral strategy, constantly updated and molded by new events.
Tim Rowe, director of the vertebrate paleontology lab at the University of Texas, was investigating the emergence of the early mammalian brain when he came up against a serious problem: there was barely any evidence to examine. Brain tissue doesn’t fossilize. Nor did the soft, cartilaginous skulls of many early mammals. Morganucodon and some later relatives had bony skulls, but the fossils they left behind were tiny, and so old they might crumble at the slightest touch. But Rowe devised a clever way around this obstacle.
In 1997, he started to use a CT scanner to create three-dimensional images of meteorites. These were crude at first, but as computing power geometrically increased in the 2000s, Rowe modeled smaller and smaller objects, focusing on early mammal fossils. He got permission to scan a Morganucodon skull. As with Mark McMenamin’s Promethean bite, Rowe found new insights in an old fossil that had been sitting on somebody’s shelf; this one occupied a lab case at Harvard, where Rowe had himself handled it twenty years earlier. Now, he gently placed it on a small table inside the scanner. It spun, and over the course of five or six hours the scanner built an image of the skull, voxel by voxel (voxels are three-dimensional pixels, the smallest components of the image). When complete, Rowe could enlarge the inch-long skull to the size of a ranch house. Studying every microscopic bump and fold in the bone, and cross-referencing it with ancient and modern anatomy, Rowe constructed a model of the brain that had occupied it, and a picture of life on the cusp of change.
The brain was 50 percent larger, relative to body size, than those of Morganucodon’s immediate ancestors; a sharpening, more expansive sense of smell accounted for most of the growth. Early mammals likely had more than a thousand distinct smell receptor genes, making them far more sensitive to scents than dinosaurs, which had perhaps a hundred. Rowe’s work suggests this was merely the first of several large pulses of smell-brain growth. He scanned another fossil skull belonging to the species Hadrocodium wui, a relative of Morganucodon that lived about 10 million years later. (Both fossils were found in China.) Hadrocodium’s skull was only about a third of an inch long, broken into dozens of nearly microscopic pieces. But once scanned and virtually reassembled, it revealed a brain almost bursting with new nerves and perceptions. It was bigger overall and its neocortex more elaborate, with more power to process and weave together all of the senses. At its base, the spinal cord bulged, suggesting more complex connections between the body and the brain, and that it moved more quickly and gracefully than its predecessors.
Echoes of this epochal transition persist in the fetal development of all mammals today. The first region to develop in a mammalian fetus’s neoc
ortex is the area that represents the mouth and tongue, because of the essential role of nursing in its survival. The earliest sensations it processes are the warmth, smell, sweet flavor, and deep gratification of mother’s milk. The first mammals had long snouts and powerful lips, as well as well-developed whiskers. The mouth and nose became more than just anatomical tools for tracking food; they made food a focal point for all experience. In the great scavenger hunt, the mouth and nose led the way.
Fruit Salad
It was just a flicker of orange, but it blazed through the green. The band of monkeys, living in the African jungle about 20 million years ago, had spent days chewing on duller fare: mostly leaves, bitter roots, and bugs, plus a few pungent berries. Suddenly, here was the hint of something great. As they clambered over tree branches, their eyes narrowed, and more flecks of orange appeared. They leaped, swinging in unison to the right spot. They grabbed the reddish-orange fruits with all five fingers, crushing them, letting the juice dribble over their hands. One squatted on a branch, leaned back against the tree’s trunk, and bit into the fruit. The sweetness exploded on his tongue, tempered by a bitterness; a brief, blinding shock of pleasure. The feast would go on until pits littered the forest floor.
The monkeys’ world would have encompassed only a few square miles, a territory probably similar in area to that of Morganucodon. They had also evolved in similar circumstances—scavenging and hiding from predators in the wake of the ecological catastrophe that killed off the dinosaurs, a giant meteor strike off the coast of the Yucatán Peninsula. But there were two crucial differences. Our ancestors’ hunt for food, formerly a ground-based affair, had moved upward into the trees. It now occupied three dimensions instead of two, and a new form of vision, paired with depth perception, rendered it in vivid colors. This advance yoked vision closely to flavor. The bright color of the forbidden fruit must have been what first caught Eve’s attention in the Garden of Eden, and this is still the case with our own meals. Colors, shapes, and the arrangement of food draw the eye and whet the appetite.
Most mammals have two-color vision: their retinas, the image-sensing area at the back of the eyeball, contain two kinds of specialized sensors called cones, with receptors that detect blue or red wavelengths of light. An animal with two-color vision can distinguish about ten thousand distinct hues. But about 23 million years ago, a gene replication occurred in a species of monkey. Those affected received a third set of cones that became tuned to the yellow band of the spectrum. Hues that had appeared flat and gray to earlier mammals now became purple, pink, sky blue, mauve, teal, coral. Reds grew deeper and subtler, greens softer and more varied. Primates with this enhanced vision, which today include some—but not all—monkey species, all apes, and humans, can detect up to a million colors. (Birds have four types of cones, and fantastically rich color vision.)
Finding fruit in a jungle setting is difficult, a “Where’s Waldo?” problem: the eye and brain must detect a distinct color signal out of the predominant hue. In the 1990s, Cambridge University neuroscientists Benedict Regan and John Mollon set out to test the fruit-vision hypothesis. They focused on red howler monkeys in the jungles of French Guiana. As if to demonstrate its own evolutionary potency, three-color vision emerged again, independently, in howler monkeys in the Americas about 13 million years ago. It’s guesswork to say what made it so successful, but there is one obvious candidate: color vision helped primates spot ripe fruit.
Howler monkeys favor the fruit of the Chrysophyllum lucentifolium tree, which have tough skins that they rip open with their teeth, and large seeds that pass through the primate digestive system. The fruits ripen to a rich blend of yellow and orange, an ideal contrast with surrounding greenery. For days a team of researchers camped out in the lowland forest, beneath a leafy canopy about a hundred feet above them. They followed groups of monkeys as they scrambled through the treetops, collecting the remains of devoured fruits.
Using a spectrometer to measure the wavelengths in the colors of the plants, the scientists found that the pigments in the retina of the howler monkey are almost perfectly attuned to the task of spotting ripe, yellow fruit amid the foliage. This was apparently no accident; the Chrysophyllum fruit’s colors occupy a very narrow band of the spectrum. Natural selection seemed to have finely tuned one to the other, producing advantages for both: food for monkeys and a way for the fruit trees to disperse their seeds. (Other foods may have also played a role: in some primates, three-color vision may have evolved to spy nutritious young red leaves among green foliage when fruits were scarce.)
Colorful fruit, then, wasn’t just a rare, tasty treat or even an important element of the prehistoric food pyramid. It was part of a broader survival strategy. The nocturnal cycles of the monkeys’ ancestors now gave way to daytime sweeps. High in the trees in the light of day, colors supplanted scents. Smell, so central in the development of intelligence and awareness, receded. Now vision took point. This tilt from one sense to the other is written into our genes: primates with three-color vision have fewer working olfactory receptor genes than those without it, meaning they can detect fewer scents.
Forests and jungles are filled with edible leaves, but fruit trees are scattered, and some bear fruit only at certain times of the year. Survival depends on some level of planning. To keep eating, an animal has to remember where the best trees are and when they’re likely to produce edible fruit. Fruit is a true prize, and it takes smarts to get it. Fruit-eating chimpanzees, bats, and parrots have bigger brains relative to body size than leaf-eating gorillas, grub-eating bats, and most other birds, respectively.
Unlike solitary Morganucodon, ancient monkeys moved and worked together as a group, communicating by sound, glance, or gesture. Superior eyesight helped here, too. Their eyes were set forward in the head, giving them three-dimensional vision—oddly, this anatomy is typical of predators, not scavengers. It puts potential prey in the center of the visual field, where it can be swiftly identified, evaluated, and attacked. But for primates, depth perception made it easier to spot the movements of stealthy, camouflaged predators, and to travel swiftly through networks of branches in low light, where one wrong move could mean a deadly fall. With just one pair of eyes, focused forward, each individual’s survival depended on the whole group acting as a unit, with multiple pairs of eyes pointing in all directions.
The demands of the hunt would have also favored ever-more-expressive faces. The brains of apes and humans have much larger visual cortices than those of other mammals relative to body size, and bigger nerve centers for making faces. Blunt expressions of fear, disgust, and pleasure present in all mammals broke loose of their roots as involuntary reflexes and added layers of individual subtlety. A glance could convey volumes. Like a band of marines, the monkeys functioned as a food-gathering unit, their feasts anticipating the present-day communal meal.
Seared Fish with Olive Garnish; Fricasseed Gazelle
In a system of basalt caves near the edge of a lake, early humans built a hearth circled by stones. Their community lived amid plenty: the lake had schools of catfish, tilapia, and carp. Crabs scuttled over the sand. Turtles meandered. On nearby hillsides, wild olives and grapes were there for the taking. The women and children would gather food and toss it into the fire. They’d watch it singe and crack, then push it out with sticks, popping the best bits into their mouths so their tongues burned, savoring the carbon-flecked flesh of fish and fruit. Men sometimes tracked and killed animals for meat, but more often they found leftovers, the remains of a deer or an elephant freshly killed by some predator. They stripped the meat and roasted it, blood and fat sizzling.
Starting about a million years ago, groups of some close relative of Homo sapiens occupied this campsite, located at the Gesher Benot Ya’aqov cave in the Hula Valley in modern Israel. It was a pleasant spot, rimmed by mountains that cooled the desert climate. Fresh water bubbled up from mountain springs and flowed into a river just to the south. Th
e groups stayed for tens of thousands of years, until a mudslide or cave-in entombed the campsite roughly 780,000 years ago. In 1935, archaeologists from the Hebrew University of Jerusalem discovered the cave and began a meticulous, decades-long excavation. They uncovered an amazing story of prehistoric dining, and a snapshot of how flavor emerged from its animal origins.
Excavators uncovered clusters of burned flint shards, as well as chunks and splinters of singed ash, oak, and olive tree branches. Studying these in the 1990s, archaeologist Naama Goren-Inbar deduced their condition could not have been the result of a random wildfire. Fires caused by lightning strikes burn briefly across wide areas, and at lower temperatures than man-made fires, which are carefully tended to focus their heat. The food items had been roasted at high temperature. The Gesher Benot Ya’aqov cave dwellers had achieved the Promethean ideal: they could control fire.
They were using it to cook. Husks of burned grains and acorn shells were also found in the main hearth area. The residents had roasted seeds from prickly water lily plants, water chestnuts, olives, wild grapes, and holy thistleberries. There were cooked fish bones and crab claws, as well as bone fragments from deer, elephants, and other animals. Fire was only the most potent of a whole suite of tools used in food preparation: these early humans had a kitchen. One area was devoted to gutting fish. A space used for processing nuts had hammerstones and pitted anvils that had been used as bases for smashing the shells of acorns before roasting them. More anvils, these used for making flint tools, were nearby.
