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Winner of the 2006 David Horrobin Prize.
Medical Hypotheses (2006), 66, 1053-1059.
Published by Elsevier.
Parental Selection: A Third Selection Process
in the Evolution of Human Hairlessness and Skin Color
Judith Rich Harris
Middletown, New Jersey, U.S.A.
Summary It is proposed that human hairlessness, and the pale skin seen in modern Europeans and Asians, are not the results of Darwinian selection; these attributes provide no survival benefits. They are instead the results of sexual selection combined with a third, previously unrecognized, process: parental selection. The use of infanticide as a method of birth control in premodern societies gave parents – in particular, mothers – the power to exert an influence on the course of human evolution by deciding whether to keep or abandon a newborn infant. If such a decision was made before the infant was born, it could be overturned in the positive direction if the infant was particularly beautiful – that is, if the infant conformed to the standards of beauty prescribed by the mother's culture. It could be overturned in the negative direction if the infant failed to meet those standards. Thus, human hairlessness and pale skin could have resulted in part from cultural preferences expressed as decisions made by women immediately after childbirth.
Those words were spoken shortly after childbirth by an African woman named Chuko, a member of the hunter-gatherer people known as the !Kung. The story was told to an anthropologist by Chuko's daughter, Nisa. Chuko had planned to kill the newborn – by burying it before it took its first breath – because her previous child, Nisa's younger brother Kumsa, was too young to be weaned. Rearing the new baby would thus jeopardize Kumsa's chances of survival. But when Chuko saw the new baby she had a change of heart. The baby was allowed to live and she did indeed grow into a beautiful girl.
Marjorie Shostak, the anthropologist who recorded Nisa's story, explained that infanticide (now against the law) was until recently the only reliable method available to !Kung women for spacing their babies. The !Kung were not unusual in their use of this draconian method of birth control. According to the evolutionary psychologist Steven Pinker, “Infanticide has been practiced in all the world's cultures” (2). In former times deciding whether to keep the newborn was often the first decision a mother had to make after she gave birth. But the decision was never made lightly, and a particularly appealing newborn had at least a slim hope of changing its mother's mind. The ethologist Irenäus Eibl-Eibesfeldt described another such incident: an Eipo woman who had decided in advance to abandon the baby if it should be a girl but changed her mind after her daughter was born (3).
A woman might make a decision not to rear a newborn either before she gave birth or afterwards. The usual reason for making the decision in advance was bad timing: the previous child had not yet been weaned, times were hard and food was scarce, or the mother lacked a partner who could help provide for the baby. When the decision was made after the birth, it was usually a reaction to the newborn itself. The infant might be the wrong sex, or appear weak and sickly, or have some kind of congenital anomaly. On the other hand, the physical appearance of the newborn might tip the balance in the other direction, in favor of life. The baby might be especially vigorous (this was the reason for the Eipo mother's change of mind) or especially beautiful (as in the case of the !Kung mother). Beauty counts, even at birth.
In writings in evolutionary biology or evolutionary psychology, the importance of beauty is usually mentioned in discussions of mate selection. Sexual selection on the basis of beauty is responsible for many of nature's glories, from the butterfly's wing to the peacock's tail (4). Sexual selection, along with the ordinary kind of Darwinian selection, based on “survival of the fittest,” are the two recognized processes that drive evolution.
In this article I propose that a third process played a role in human evolution: parental (usually maternal) selection. Though the decision to rear or abandon a newborn was made in only a small percentage of cases, it was made again and again, over a period of more than 100,000 years. During that period the decision would have been made often enough to exert an influence on the observable characteristics of our species.
A similar process of selection by human choice was involved in the breeding of domesticated animals and was responsible for the changes that distinguished them from their wild ancestors. The main difference was that animal breeders could wait for many months before deciding whether a particular dog or horse was or was not satisfactory. The decision about whether or not to rear an infant human, on the other hand, could ordinarily be made only at its birth. Once the mother had held the infant in her arms and nursed it, it was almost always too late: the decision had already been made. Thus, the characteristics that could tip the balance one way or another for a human infant had to be visible at its birth. Two such characteristics are the newborn's skin color (as in the case of the !Kung baby) and its hairiness or hairlessness.
I propose that human hairlessness and the pale skin seen in the Northern members of our species are the results, at least in part, of parental selection. Sexual selection no doubt played a role as well, but parental selection could have speeded things up, thereby producing very noticeable changes in relatively brief periods of evolutionary time (as was true in the case of domesticated animals).
The hairless ape
Many theories, some quite outlandish, have been advanced to account for the fact that, of all extant primates, Homo sapiens is the only one lacking a protective coat of fur. Most of these theories are attempts to explain our loss of hair on a survival-of-the-fittest basis; the idea is that hairlessness somehow increased our fitness in the hot and sunny climate of Africa in which our species emerged. But other mammals of similar size – baboons, chimpanzees, gorillas, impalas, gazelles, hyenas, leopards, cheetahs – have managed to survive quite well in Africa despite being covered with fur.
Paintings and exhibits on human evolution often feature a line-up of increasingly humanlike creatures, starting from some apish ancestor, progressing through Homo habilis and Homo erectus, and ending up triumphantly at Homo sapiens. Along the way these creatures become progressively less hairy, like a commercial for a baldness remedy played in reverse. I maintain that these paintings and exhibits are misleading and that Homo sapiens, perhaps along with its immediate (unknown) predecessor, were the only naked primates in our evolutionary line. I propose that Homo erectus and its Northern descendant, Neanderthal, were as furry as any other ape.
Neanderthals never could have survived for many thousands of years in Ice-Age Europe and Asia without a heavy coat of fur. In its other characteristics – those we can judge from its bony remains, which are all that are currently available to us – Neanderthal showed clear signs of adaptation to a cold climate: thick body, shortened limbs (5). The fact that Neanderthals probably possessed the skill of using fire is not enough to explain their survival through all those years of freezing cold. Are we to suppose that they spent all their time huddling by the fire? Impossible, because they lived mostly on meat. They had to go out to hunt every few days, and the game they sought did not linger conveniently by the entrance to their cave.
The important question is not whether Neanderthals had fire but whether they had the needle – whether they could sew. A deer skin slung over the shoulders would have been inadequate protection against Ice-Age chill.
The needle is part of the Upper Paleolithic toolkit – part of the “cultural revolution” that dates from around 50,000 years ago. Evidence on the evolution of the human body louse, an insect that lives in human clothing, also supports the view that clothing was invented around 50,000 years ago (6). The tools associated with Neanderthals, which underwent little change during the many thousands of years in which they ruled Europe and Asia are, in contrast, Middle Paleolithic (7). The evidence strongly suggests that Neanderthals did not invent or use the needle and that they could not sew. Even if they had adopted the use of needles at the time they were first introduced, that would not explain how they managed to survive in the Northern Hemisphere during the previous 70 or 80 millennia without a coat of fur. All the other mammals that made it through the Ice Age – the mammoth, for instance – were furry.
The mammoth's relatives in Africa were as naked as humans are today. Thus, it is possible that Homo erectus – the common ancestor of Neanderthal and Homo sapiens – was also naked or semi-naked, and that fur re-evolved in Neanderthals when climate change made it necessary. I cannot rule out this hypothesis but the evidence does not favor it. Other large mammals found in Africa – notably the rhinoceros – are largely naked; but all the other medium-sized African mammals are furred. Some force other than selection on the basis of fitness appears to have been responsible for our hairlessness.
That force, I believe, was culture. Thus, the evolution of hairlessness would have had as one of its prerequisites a brain large and fancy enough, not just to produce cultures, but to make them a potent force in determining who lives and who dies.
The change could have occurred over a relatively short period of time if one group of hominids adopted the cultural belief that they were people and that any living thing with fur on it was an animal – hence, prey. The idea that “we alone are people” is common among tribal societies; a tribe's name for itself often translates as “the people.” An Amazonian group, the Wari, go even further: their language has a special term for edible things and they apply it to anyone who is not a Wari (8).
Once the notion that “hairlessness is us, hairiness is them” became part of the culture of a group of hominids, then sexual selection plus parental selection could have eliminated hairiness very quickly. Any infant born too hairy would have elicited an “ugh” response; in all likelihood, it would have been killed or abandoned at birth. A gene for hairiness would have been, in effect, lethal.
But is there in fact a gene for hairiness? Yes, the evidence suggests that a change in a single gene, or in a small number of genes, could have been responsible for the loss of our pelage. A rare condition called congenital hypertrichosis universalis, also known as Ambras syndrome, occasionally turns up in modern humans. Here is a description from a medical journal of an infant with this condition:
(If you can imagine delivering, or being presented with, an infant matching this description, you might find that the “ugh” response has not entirely disappeared.)
Ambras syndrome occasionally appears in two siblings in the same family. Genetic studies have attributed this mutation to autosomal recessive inheritance or to germline mosaicism for an autosomal dominant gene, which would imply that a single gene was involved (10). Other researchers have traced the condition to an inversion of a portion of chromosome 8 (11). This finding is not inconsistent with the notion that a single gene is involved; the rearrangement of chromosome 8 might have separated the gene from the section of DNA that normally switches it on or off. In other words, we might still have the gene for hairiness but it is normally not expressed in the members of our species.
If I am correct in hypothesizing that Neanderthals were as furry as the other mammals that made it through the Ice Age in Europe and Asia, then this hypothesis would provide an explanation for their disappearance, shortly after Homo sapiens appeared on the scene. To a hungry human, a hairy Neanderthal would be seen as animal – hence, as prey. In Africa today, hungry humans dine on the flesh of chimpanzees and gorillas. The Neanderthals, I propose, disappeared from Europe and Asia for the same reason that the mammoths disappeared: we ate them. We won the battle for the possession of Europe and Asia – a battle between two different species of meat-eaters – because we had better brains and a better toolkit. We are here and the Neanderthals are not because we were better predators than they were.
Could a Neanderthal pass?
A game that paleoanthropologists sometimes like to play is to fantasize about a male Neanderthal who appears on the streets of New York or London, dressed up in a three-piece suit. Will he be noticed or can he pass as human?
The problem is that the paleoanthropologists have forgotten to shave him. Of course he will be noticed: He will be shot with a tranquilizer dart and carted off to the zoo. But his hairiness is only one of his problems; the other is the three-piece suit. The Neanderthal lacked a needle. His tailoring skills could not even provide him with a warm parka, much less a three-piece suit.
The pale ape
If I am correct in proposing that hairlessness is a characteristic only of our species of primate, then it would have arisen no longer ago than 200,000 years. The pale skin seen in humans whose ancestors came from Europe or Asia is an even more recent innovation and must have occurred over an even shorter period of evolutionary time. In this case, there is little disagreement over timing: Pale skin could not have appeared before Homo sapiens began to spread across the Northern Hemisphere, an event that probably occurred no more than 40,000 or 50,000 years ago.
Pale skin would have had negative survival value in hot, sunny Africa. This characteristic could – and evidently did – evolve only in climes that were cool and cloudy enough to make it less of a handicap. In far northern regions, paleness might even have provided some benefit, by enabling the skin to synthesize Vitamin D even when the sun was not overhead or was partly obscured by clouds.
But by making the paler members of our species vulnerable to sunburn and malignant melanoma, in most environments the negative consequences of light skin would have outweighed the positives. The combination of hairlessness and depigmentation has produced a mammal that takes its life in its hands whenever it ventures into the noonday sun.
And yet there is a cultural preference, noticeable today in most societies around the world and expressed in the quote from Nisa's mother at the beginning of this article, for pale skin. The fact that this preference is widespread – perhaps even universal in our species – suggests that it did not arise recently. If this preference has long historical roots, it could be responsible for the paleness that can be seen today in people whose ancestors lived in places in which pale skin was not a serious handicap.
I would like to look more closely at the cultural preference for light skin because it has often been misunderstood. Take, for example, a recent article in Time, titled “Could You Please Make Me a Shade Lighter?” (12). The article is about the preference for light skin seen in India today. The preference is so strong that a dark-skinned Indian woman has virtually no hope of becoming a movie star or model; even finding someone to marry is a problem for her. According to the author of the article, “Asia, from its geishas to its Ganesha gods, has always prized the pale.” The author gamely tries to provide an explanation for this preference, noting that “dark skin is associated with lowly labor in the outdoors.” But what he has missed is that the preference is for pale females: female models, female geishas, female wives. For males to be dark is all right or at least much less of a handicap.
Other writers have been confused by the fact that, for a period of forty or fifty years in the latter part of the 20th century, Americans and Europeans of both sexes basked in the sun in order to acquire a tan. I believe this was simply a fad – a cultural aberration – similar to the current craze for muscle-building (which is also seen in people of both sexes). Aside from this one period in which a tanned body was associated with the leisure class, there has generally been a preference for pale-skinned women. Throughout human history, women – but not men – have sought protection from the sun. In ancient Greece and Rome, umbrellas (the word means “a little shadow”) or parasols (“for the sun”) were used for this purpose. This device was so closely associated with the female sex that its use by a male was seen as effeminate (13).
The American novel Gone With the Wind, published in 1936 and set in the mid-1800s in the southern United States, depicts the typical attitude toward pale skin and tanning in females. The book opens with a scene in which the heroine, Scarlett O'Hara, is flirting with two young men. Here is how Scarlett is described:
The two young men, in contrast, are described as having “sunburned faces.” It was apparently all right, in the antebellum South, for males to be sunburned or to have naturally dark skin; indeed, dark skin in males was seen as attractive (hence the description of the ideal man as “tall, dark and handsome”). Here is the description given of Rhett Butler – the love of Scarlett's life – when he first appears on the scene:
Lest the reader wonder whether Rhett might be a trifle too dark and jump to the wrong conclusion, the author is quick to provide reassurance:
Why would light skin be favored in females but not in males? My hypothesis here is based on such slender evidence that it probably should be called a guess. Many of the female characteristics that are favored by males in mate selection are associated with youthfulness: firm breasts, smooth skin, pink cheeks, full lips, small waist (16). I found my clue on the cover of Jane Goodall's book, The Chimpanzees of Gombe (17). The photo on the cover shows three chimpanzees, an infant and two adults. The infant's skin, which is plainly visible on its face and ears because these areas are not fur-covered, is as pale as that of a Norwegian; the skin of the adults is as dark as that of a Nigerian. According to Goodall, skin color is a cue to a chimpanzee's age and is used as such by other chimpanzees. This animal is born with pale skin that darkens as it matures.
Our ancestors parted company with the ancestors of the modern chimpanzee between 5 and 7 million years ago. If our last common ancestor had the same characteristic as the modern chimp – skin that is pale at birth and gradually darkens – then paleness of skin might have been used as a criterion in mate selection, just as firm breasts and a small waist are today. Thus, the male preference for pale-skinned females might be very ancient. It might predate, not only the appearance of a primate smart enough to use a needle, but the appearance of a primate who could walk erect.
The male preference for pale-skinned females – sexual selection – could have led to the evolution of a preference, in parents, for pale-skinned daughters. It is adaptive (in the Darwinian sense) for parents to favor characteristics in their offspring that give these offspring an advantage in the mating game and to distribute their parental investment accordingly. If pale-skinned daughters are preferred by males, then these daughters can be more choosy in mate selection, thereby giving their parents higher-quality grandchildren. The evolutionary biologist Helena Cronin used a similar argument to explain why a female peacock, say, should go along with the majority preference and choose a mate with a long tail even though the tail is an impediment: “In a population in which there is a majority preference for anything whatsoever, a female would do best to follow the fashion, however arbitrary, however absurd, because the next generation of daughters will inherit their mothers' preference whilst her sons will inherit their father's attractive feature” (18). In the same way, the offspring of the pale-skinned mother and the father with a preference for pale-skinned females have a good chance of inheriting their mother's skin color and/or their father's preference for pale skin.
The history of the umbrella
Cronin contrasts “good sense” evolution, based on survival considerations, with “good taste” evolution, based on considerations of beauty or fashion. Good taste evolution is produced, in her view, by sexual selection. I believe that parental selection also plays a role in good taste evolution. Sexual selection can produce fairly rapid changes in a species, but sexual selection plus parental selection – the two generally work hand in hand, for the reason just noted – can produce dramatic changes with dazzling speed.
It was these two forces working together – first in selection for hairlessness, later in selection (in the Northern branch of our species) for lightness of skin, that produced the pale-skinned, hairless ape that today walks the streets of New York, London, and Copenhagen. This pathetic creature has, of necessity, long been seeking protection from the sun. The umbrella (or parasol) has been in use for at least 4000 years. For most of that time, as I mentioned, it has been used mostly by women and almost exclusively to ward off the sun, rather than the rain. The first English men who used the umbrella to protect themselves against rain – this was in the mid-1700s – were ridiculed for being effeminate or mocked by being called “Frenchman.” (Yes, even in the 1700s the French were depicted as effete by English speakers.)
But Robinson Crusoe, in the privacy of his tropical island, had the luxury of being able to use an umbrella for both purposes, sun and rain, without fear of being mocked. (There was nobody around but Friday and what did Friday know?) Robinson Crusoe was a fictional character but Daniel Defoe's book, published in 1719, was based on a real historical incident. Here is how Defoe described Crusoe's construction of an umbrella:
Notice that Crusoe discovered that a hide covered with fur provided good protection against both sun and rain, against both heat and cold. A coat of fur also provides some protection against cuts and abrasion. It was our ancestors' pride in being humans that robbed us of this handy attribute and left us naked in the noonday sun.
Testing the hypotheses
To be testable, a hypothesis has to be disprovable. There is a straightforward way to disprove my hypothesis about the evolution of hairlessness: find the corpse of a Neanderthal that had been frozen in a glacier for 30,000 years or more. If its body is as well-preserved as that of the 5,000-year-old corpse of the “Ice Man” found in the Alps in 1992, then the question of whether Neanderthals were furry will be easy to answer. A hairless, long-dead Neanderthal would provide definitive evidence against my hypothesis. I would, of course, be delighted by the discovery of a furry, dead Neanderthal, and more delighted still by the unexpected appearance of a live one.
But a live, furry Neanderthal, or even remains in which the soft tissues have been preserved, is probably too much to hope for. Fortunately, there are other ways of obtaining evidence for or against my hypothesis. Such evidence could be sought in newer methods of genetic analysis that provide information about how long ago and how rapidly evolutionary changes occurred in the genes, and which genes evolved together. My prediction is that the change to hairlessness occurred far more recently and far more rapidly than has heretofore been believed.
My hypothesis about the evolution of pale skin is a good deal more difficult to test. No one doubts that this change must have occurred after members of our species occupied Europe and Asia; as far as I know, no one doubts that it occurred after our species developed language and culture. Thus, my hypothesis does not differ from prevailing views in regard to timing. Soft-tissue evidence from frozen ice men will be of no use.
Evidence will therefore have to sought in a roundabout way. For example, I asserted that light skin provided no survival benefits to the ancestors of modern-day Europeans. If it is found that modern light-skinned humans have longer or healthier lives than their darker-skinned neighbors, at least at some latitudes, that would be evidence against my hypothesis. Another prediction is that females should, on average, have lighter skin than males. There already appears to be enough evidence that light-skinned females win higher-quality mates – males with higher status – than their darker-skinned sisters.
Alas, the beautiful fair-skinned baby whom Nisa's mother decided to rear, rather than kill, cannot provide us with any evidence, pro or con. Kxamshe, as she was called, died in her early teens, apparently of malaria (20).