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May 2001

Mothers and Others

From queen bees to elephant matriarchs, many animal mothers are assisted by others in rearing offspring. Anthropologist Sarah Blaffer Hrdy maintains that our human ancestors, too, were “cooperative breeders”—a mode of life that enabled them to thrive in many new environments. Today, argues Hrdy, our continued ability to raise emotionally healthy children may well depend on how well we understand the cooperative aspect of our evolutionary heritage.

This article was adapted from �Cooperation, Empathy, and the Needs of Human infants,� a Tanner Lecture delivered at the University of Utah. It is used with permission of the Tanner Lectures on Human Values, a Corporation, University of Utah, Salt lake City.

Mother apes—chimpanzees, gorillas, orangutans, humans—dote on their babies. And why not? They give birth to an infant after a long gestation and, in most cases, suckle it for years. With humans, however, the job of providing for a juvenile goes on and on. Unlike all other ape babies, ours mature slowly and reach independence late. A mother in a foraging society may give birth every four years or so, and her first few children remain dependent long after each new baby arrives; among nomadic foragers, grown-ups may provide food to children for eighteen or more years. To come up with the 10–13 million calories that anthropologists such as Hillard Kaplan calculate are needed to rear a young human to independence, a mother needs help.

So how did our prehuman and early human ancestresses living in the Pleistocene Epoch (from 1.6 million until roughly 10,000 years ago) manage to get those calories? And under what conditions would natural selection allow a female ape to produce babies so large and slow to develop that they are beyond her means to rear on her own?

The old answer was that fathers helped out by hunting. And so they do. But hunting is a risky occupation, and fathers may die or defect or take up with other females. And when they do, what then? New evidence from surviving traditional cultures suggests that mothers in the Pleistocene may have had a significant degree of help—from men who thought they just might have been the fathers, from grandmothers and great-aunts, from older children.

These helpers other than the mother, called allomothers by sociobiologists, do not just protect and provision youngsters. In groups such as the Efe and Aka Pygmies of central Africa, allomothers actually hold children and carry them about. In these tight-knit communities of communal foragers—within which men, women, and children still hunt with nets, much as humans are thought to have done tens of thousands of years ago—siblings, aunts, uncles, fathers, and grandmothers hold newborns on the first day of life. When University of New Mexico anthropologist Paula Ivey asked an Efe woman, “Who cares for babies?” the immediate answer was, “We all do!” By three weeks of age, the babies are in contact with allomothers 40 percent of the time. By eighteen weeks, infants actually spend more time with allomothers than with their gestational mothers. On average, Efe babies have fourteen different caretakers, most of whom are close kin. According to Washington State University anthropologist Barry Hewlett, Aka babies are within arm’s reach of their fathers for more than half of every day.

Accustomed to celebrating the antiquity and naturalness of mother-centered models of child care, as well as the nuclear family in which the mother nurtures while the father provides, we Westerners tend to regard the practices of the Efe and the Aka as exotic. But to sociobiologists, whose stock in trade is comparisons across species, all this helping has a familiar ring. It’s called cooperative breeding. During the past quarter century, as anthropologists and sociobiologists started to compare notes, one of the spectacular surprises has been how much allomaternal care goes on, not just within various human societies but among animals generally. Evidently, diverse organisms have converged on cooperative breeding for the best of evolutionary reasons.

A broad look at the most recent evidence has convinced me that cooperative breeding was the strategy that permitted our own ancestors to produce costly, slow-maturing infants at shorter intervals, to take advantage of new kinds of resources in habitats other than the mixed savanna-woodland of tropical Africa, and to spread more widely and swiftly than any primate had before. We already know that animal mothers who delegate some of the costs of infant care to others are thereby freed to produce more or larger young or to breed more frequently. Consider the case of silver-backed jackals. Patricia Moehlman, of the World Conservation Union, has shown that for every extra helper bringing back food, jackal parents rear one extra pup per litter. Cooperative breeding also helps various species expand into habitats in which they would normally not be able to rear any young at all. Florida scrub-jays, for example, breed in an exposed landscape where unrelenting predation from hawks and snakes usually precludes the fledging of young; survival in this habitat is possible only because older siblings help guard and feed the young. Such cooperative arrangements permit animals as different as naked mole rats (the social insects of the mammal world) and wolves to move into new habitats and sometimes to spread over vast areas.

What does it take to become a cooperative breeder? Obviously, this lifestyle is an option only for creatures capable of living in groups. It is facilitated when young but fully mature individuals (such as young Florida scrub-jays) do not or cannot immediately leave their natal group to breed on their own and instead remain among kin in their natal location. As with delayed maturation, delayed dispersal of young means that teenagers, “spinster” aunts, real and honorary uncles will be on hand to help their kin rear young. Flexibility is another criterion for cooperative breeders. Helpers must be ready to shift to breeding mode should the opportunity arise. In marmosets and tamarins—the little South American monkeys that are, besides us, the only full-fledged cooperative breeders among primates—a female has to be ready to be a helper this year and a mother the next. She may have one mate or several. In canids such as wolves or wild dogs, usually only the dominant, or alpha, male and female in a pack reproduce, but younger group members hunt with the mother and return to the den to regurgitate predigested meat into the mouths of her pups. In a fascinating instance of physiological flexibility, a subordinate female may actually undergo hormonal transformations similar to those of a real pregnancy: her belly swells, and she begins to manufacture milk and may help nurse the pups of the alpha pair. Vestiges of cooperative breeding crop up as well in domestic dogs, the distant descendants of wolves. After undergoing a pseudopregnancy, my neighbors’ Jack Russell terrier chased away the family’s cat and adopted and suckled her kittens. To suckle the young of another species is hardly what Darwinians call an adaptive trait (because it does not contribute to the surrogate’s own survival). But in the environment in which the dog family evolved, a female’s tendency to respond when infants signaled their need—combined with her capacity for pseudopregnancy—would have increased the survival chances for large litters born to the dominant female.

According to the late W.D. Hamilton, evolutionary logic predicts that an animal with poor prospects of reproducing on his or her own should be predisposed to assist kin with better prospects so that at least some of their shared genes will be perpetuated. Among wolves, for example, both male and female helpers in the pack are likely to be genetically related to the alpha litter and to have good reasons for not trying to reproduce on their own: in a number of cooperatively breeding species (wild dogs, wolves, hyenas, dingoes, dwarf mongooses, marmosets), the helpers do try, but the dominant female is likely to bite their babies to death. The threat of coercion makes postponing ovulation the better part of valor, the least-bad option for females who must wait to breed until their circumstances improve, either through the death of a higher-ranking female or by finding a mate with an unoccupied territory.

One primate strategy is to line up extra fathers. Among common marmosets and several species of tamarins, females mate with several males, all of which help rear her young. As primatologist Charles T. Snowdon points out, in three of the four genera of Callitrichidae (Callithrix, Saguinus, and Leontopithecus), the more adult males the group has available to help, the more young survive. Among many of these species, females ovulate just after giving birth, perhaps encouraging males to stick around until after babies are born. (In cotton-top tamarins, males also undergo hormonal changes that prepare them to care for infants at the time of birth.) Among cooperative breeders of certain other species, such as wolves and jackals, pups born in the same litter can be sired by different fathers.

Human mothers, by contrast, don’t ovulate again right after birth, nor do they produce offspring with more than one genetic father at a time. Ever inventive, though, humans solve the problem of enlisting help from several adult males by other means. In some cultures, mothers rely on a peculiar belief that anthropologists call partible paternity—the notion that a fetus is built up by contributions of semen from all the men with whom women have had sex in the ten months or so prior to giving birth. Among the Canela, a matrilineal tribe in Brazil studied for many years by William Crocker of the Smithsonian Institution, publicly sanctioned intercourse between women and men other than their husbands—sometimes many men—takes place during villagewide ceremonies. What might lead to marital disaster elsewhere works among the Canela because the men believe in partible paternity. Across a broad swath of South America—from Paraguay up into Brazil, westward to Peru, and northward to Venezuela—mothers rely on this convenient folk wisdom to line up multiple honorary fathers to help them provision both themselves and their children. Over hundreds of generations, this belief has helped children thrive in a part of the world where food sources are unpredictable and where husbands are as likely as not to return from the hunt empty-handed.

The Bari people of Venezuela are among those who believe in shared paternity, and according to anthropologist Stephen Beckerman, Bari children with more than one father do especially well. In Beckerman’s study of 822 children, 80 percent of those who had both a “primary” father (the man married to their mother) and a “secondary” father survived to age fifteen, compared with 64 percent survival for those with a primary father alone. Not surprisingly, as soon as a Bari woman suspects she is pregnant, she accepts sexual advances from the more successful fishermen or hunters in her group. Belief that fatherhood can be shared draws more men into the web of possible paternity, which effectively translates into more food and more protection.

But for human mothers, extra mates aren’t the only source of effective help. Older children, too, play a significant role in family survival. University of Nebraska anthropologists Patricia Draper and Raymond Hames have just shown that among !Kung hunters and gatherers living in the Kalahari Desert, there is a significant correlation between how many children a parent successfully raises and how many older siblings were on hand to help during that person’s own childhood.

Older matrilineal kin may be the most valuable helpers of all. University of Utah anthropologists Kristen Hawkes and James O’Connell and their UCLA colleague Nicholas Blurton Jones, who have demonstrated the important food-gathering role of older women among Hazda hunter-gatherers in Tanzania, delight in explaining that since human life spans may extend for a few decades after menopause, older women become available to care for—and to provide vital food for—children born to younger kin. Hawkes, O’Connell, and Blurton Jones further believe that dating from the earliest days of Homo erectus, the survival of weaned children during food shortages may have depended on tubers dug up by older kin.

At various times in human history, people have also relied on a range of customs, as well as on coercion, to line up allomaternal assistance—for example, by using slaves or hiring poor women as wet nurses. But all the helpers in the world are of no use if they’re not motivated to protect, carry, or provision babies. For both humans and nonhumans, this motivation arises in three main ways: through the manipulation of information about kinship; through appealing signals coming from the babies themselves; and, at the heart of it all, from the endocrinological and neural processes that induce individuals to respond to infants’ signals. Indeed, all primates and many other mammals eventually respond to infants in a nurturing way if exposed long enough to their signals. Trouble is, “long enough” can mean very different things in males and females, with their very different response thresholds.

For decades, animal behaviorists have been aware of the phenomenon known as priming. A mouse or rat encountering a strange pup is likely to respond by either ignoring the pup or eating it. But presented with pup after pup, rodents of either sex eventually become sensitized to the baby and start caring for it. Even a male may gather pups into a nest and lick or huddle over them. Although nurturing is not a routine part of a male’s repertoire, when sufficiently primed he behaves as a mother would. Hormonal change is an obvious candidate for explaining this transformation. Consider the case of the cooperatively breeding Florida scrub-jays studied by Stephan Schoech, of the University of Memphis. Prolactin, a protein hormone that initiates the secretion of milk in female mammals, is also present in male mammals and in birds of both sexes. Schoech showed that levels of prolactin go up in a male and female jay as they build their nest and incubate eggs and that these levels reach a peak when they feed their young. Moreover, prolactin levels rise in the jays’ nonbreeding helpers and are also at their highest when they assist in feeding nestlings.

As it happens, male, as well as immature and nonbreeding female, primates can respond to infants’ signals, although quite different levels of exposure and stimulation are required to get them going. Twenty years ago, when elevated prolactin levels were first reported in common marmoset males (by Alan Dixson, for Callithrix jacchus), many scientists refused to believe it. Later, when the finding was confirmed, scientists assumed this effect would be found only in fathers. But based on work by Scott Nunes, Jeffrey Fite, Jeffrey French, Charles Snowdon, Lucille Roberts, and many others—work that deals with a variety of species of marmosets and tamarins—we now know that all sorts of hormonal changes are associated with increased nurturing in males. For example, in the tufted-eared marmosets studied by French and colleagues, testosterone levels in males went down as they engaged in caretaking after the birth of an infant. Testosterone levels tended to be lowest in those with the most paternal experience.

The biggest surprise, however, has been that something similar goes on in males of our own species. Anne Storey and colleagues in Canada have reported that prolactin levels in men who were living with pregnant women went up toward the end of the pregnancy. But the most significant finding was a 30 percent drop in testosterone in men right after the birth. (Some endocrinologically literate wags have proposed that this drop in testosterone levels is due to sleep deprivation, but this would probably not explain the parallel testosterone drop in marmoset males housed with parturient females.) Hormonal changes during pregnancy and lactation are, of course, indisputably more pronounced in mothers than in the men consorting with them, and no one is suggesting that male consorts are equivalent to mothers. But both sexes are surprisingly susceptible to infant signals—explaining why fathers, adoptive parents, wet nurses, and day-care workers can become deeply involved with the infants they care for.

Genetic relatedness alone, in fact, is a surprisingly unreliable predictor of love. What matters are cues from infants and how these cues are processed emotionally. The capacity for becoming emotionally hooked—or primed—also explains how a fully engaged father who is in frequent contact with his infant can become more committed to the infant’s well-being than a detached mother will.

But we can’t forget the real protagonist of this story: the baby. From birth, newborns are powerfully motivated to stay close, to root—even to creep—in quest of nipples, which they instinctively suck on. These are the first innate behaviors that any of us engage in. But maintaining contact is harder for little humans to do than it is for other primates. One problem is that human mothers are not very hairy, so a human mother not only has to position the baby on her breast but also has to keep him there. She must be motivated to pick up her baby even before her milk comes in, bringing with it a host of hormonal transformations.

Within minutes of birth, human babies can cry and vocalize just as other primates do, but human newborns can also read facial expressions and make a few of their own. Even with blurry vision, they engage in eye-to-eye contact with the people around them. Newborn babies, when alert, can see about eighteen inches away. When people put their faces within range, babies may reward this attention by looking back or even imitating facial expressions. Orang and chimp babies, too, are strongly attached to and interested in their mothers’ faces. But unlike humans, other ape mothers and infants do not get absorbed in gazing deeply into each other’s eyes.

To the extent that psychiatrists and pediatricians have thought about this difference between us and the other apes, they tend to attribute it to human mental agility and our ability to use language. Interactions between mother and baby, including vocal play and babbling, have been interpreted as protoconversations: revving up the baby to learn to talk. Yet even babies who lack face-to-face stimulation—babies born blind, say—learn to talk. Furthermore, humans are not the only primates to engage in the continuous rhythmic streams of vocalization known as babbling. Interestingly, marmoset and tamarin babies also babble. It may be that the infants of cooperative breeders are specially equipped to communicate with caretakers. This is not to say that babbling is not an important part of learning to talk, only to question which came first—babbling so as to develop into a talker, or a predisposition to evolve into a talker because among cooperative breeders, babies that babble are better tended and more likely to survive.

If humans evolved as cooperative breeders, the degree of a human mother’s commitment to her infant should be linked to how much social support she herself can expect. Mothers in cooperatively breeding primate species can afford to bear and rear such costly offspring as they do only if they have help on hand. Maternal abandonment and abuse are very rarely observed among primates in the wild. In fact, the only primate species in which mothers are anywhere near as likely to abandon infants at birth as mothers in our own species are the other cooperative breeders. A study of cotton-top tamarins at the New England Regional Primate Research Center showed a 12 percent chance of abandonment if mothers had older siblings on hand to help them rear twins, but a 57 percent chance when no help was available. Overburdened mothers abandoned infants within seventy-two hours of birth.

This new way of thinking about our species’ history, with its implications for children, has made me concerned about the future. So far, most Western researchers studying infant development have presumed that living in a nuclear family with a fixed division of labor (mom nurturing, dad providing) is the normal human adaptation. Most contemporary research on children’s psychosocial development is derived from John Bowlby’s theories of attachment and has focused on such variables as how available and responsive the mother is, whether the father is present or absent, and whether the child is in the mother’s care or in day care. Sure enough, studies done with this model in mind always show that children with less responsive mothers are at greater risk.

It is the baby, first and foremost, who senses how available and how committed its mother is. But I know of no studies that take into account the possibility that humans evolved as cooperative breeders and that a mother’s responsiveness also happens to be a good indicator of her social supports. In terms of developmental outcomes, the most relevant factor might not be how securely or insecurely attached to the mother the baby is—the variable that developmental psychologists are trained to measure—but rather how secure the baby is in relation to all the people caring for him or her. Measuring attachment this way might help explain why even children whose relations with their mother suggest they are at extreme risk manage to do fine because of the interventions of a committed father, an older sibling, or a there-when-you-need-her grandmother.

The most comprehensive study ever done on how nonmaternal care affects kids is compatible with both the hypothesis that humans evolved as cooperative breeders and the conventional hypothesis that human babies are adapted to be reared exclusively by mothers. Undertaken by the National Institute of Child Health and Human Development (NICHD) in 1991, the seven-year study included 1,364 children and their families (from diverse ethnic and economic backgrounds) and was conducted in ten different U.S. locations. This extraordinarily ambitious study was launched because statistics showed that 62 percent of U.S. mothers with children under age six were working outside the home and that the majority of them (willingly or unwillingly) were back at work within three to five months of giving birth. Because this was an entirely new social phenomenon, no one really knew what the NICHD’s research would reveal.

The study’s main finding was that both maternal and hired caretakers’ sensitivity to infant needs was a better predictor of a child’s subsequent development and behavior (such traits as social “compliance,” respect for others, and self-control were measured) than was actual time spent apart from the mother. In other words, the critical variable was not the continuous presence of the mother herself but rather how secure infants felt when cared for by someone else. People who had been convinced that babies need full-time care from mothers to develop normally were stunned by these results, while advocates of day care felt vindicated. But do these and other, similar findings mean that day care is not something we need to worry about anymore?

Not at all. We should keep worrying. The NICHD study showed only that day care was better than mother care if the mother was neglectful or abusive. But excluding such worst-case scenarios, the study showed no detectable ill effects from day care only when infants had a secure relationship with parents to begin with (which I take to mean that babies felt wanted) and only when the day care was of high quality. And in this study’s context, “high quality” meant that the facility had a high ratio of caretakers to babies, that it had the same caretakers all the time, and that the caretakers were sensitive to infants’ needs—in other words, that the day care staff acted like committed kin.

Bluntly put, this kind of day care is almost impossible to find. Where it exists at all, it’s expensive. Waiting lists are long, even for cheap or inadequate care. The average rate of staff turnover in day care centers is 30 percent per year, primarily because these workers are paid barely the minimum wage (usually less, in fact, than parking-lot attendants). Furthermore, day care tends to be age-graded, so even at centers where staff members stay put, kids move annually to new teachers. This kind of day care is unlikely to foster trusting relationships.

What conclusion can we draw from all this? Instead of arguing over “mother care” versus “othercare,” we need to make day care better. And this is where I think today’s evolution-minded researchers have something to say. Impressed by just how variable child-rearing conditions can be in human societies, several anthropologists and psychologists (including Michael Lamb, Patricia Draper, Henry Harpending, and James Chisholm) have suggested that babies are up to more than just maintaining the relationship with their mothers. These researchers propose that babies actually monitor mothers to gain information about the world they have been born into. Babies ask, in effect, Is this world filled with people who are going to provide for me and help me survive? Can I count on them to care about me? If the answer to those questions is yes, they begin to sense that developing a conscience and a capacity for compassion would be a great idea. If the answer is no, they may then be asking, Can I not afford to count on others? Would I be better off just grabbing what I need, however I can? In this case, empathy, or thinking about others’ needs, would be more of a hindrance than a help.

For a developing baby and child, the most practical way to behave might vary drastically, depending on whether the mother has kin who help, whether the father is around, whether foster parents are well-meaning or exploitative. These factors, however unconsciously perceived by the child, affect important developmental decisions. Being extremely self-centered or selfish, being oblivious to others or lacking in conscience—traits that psychologists and child-development theorists may view as pathological—are probably quite adaptive traits for an individual who is short on support from other group members.

If I am right that humans evolved as cooperative breeders, Pleistocene babies whose mothers lacked social support and were less than fully committed to infant care would have been unlikely to survive. But once people started to settle down—10,000 or 20,000 or perhaps 30,000 years ago—the picture changed. Ironically, survival chances for neglected children increased. As people lingered longer in one place, eliminated predators, built walled houses, stored food—not to mention inventing things such as rubber nipples and pasteurized milk—infant survival became decoupled from continuous contact with a caregiver.

Since the end of the Pleistocene, whether in preindustrial or industrialized environments, some children have been surviving levels of social neglect that previously would have meant certain death. Some children get very little attention, even in the most benign of contemporary homes. In the industrialized world, children routinely survive caretaking practices that an Efe or a !Kung mother would find appallingly negligent. In traditional societies, no decent mother leaves her baby alone at any time, and traditional mothers are shocked to learn that Western mothers leave infants unattended in a crib all night.

Without passing judgment, one may point out that only in the recent history of humankind could infants deprived of supportive human contact survive to reproduce themselves. Certainly there are a lot of humanitarian reasons to worry about this situation: one wants each baby, each child, to be lovingly cared for. From my evolutionary perspective, though, even more is at stake.

Even if we manage to survive what most people are worrying about—global warming, emergent diseases, rogue viruses, meteorites crashing into earth—will we still be human thousands of years down the line? By that I mean human in the way we currently define ourselves. The reason our species has managed to survive and proliferate to the extent that 6 billion people currently occupy the planet has to do with how readily we can learn to cooperate when we want to. And our capacity for empathy is one of the things that made us good at doing that.

At a rudimentary level, of course, all sorts of creatures are good at reading intentions and movements and anticipating what other animals are going to do. Predators from gopher snakes to lions have to be able to anticipate where their quarry will dart. Chimps and gorillas can figure out what another individual is likely to know or not know. But compared with that of humans, this capacity to entertain the psychological perspective of other individuals is crude.

The capacity for empathy is uniquely well developed in our species, so much so that many people (including me) believe that along with language and symbolic thought, it is what makes us human. We are capable of compassion, of understanding other people’s “fears and motives, their longings and griefs and vanities,” as novelist Edmund White puts it. We spend time and energy worrying about people we have never even met, about babies left in dumpsters, about the existence of more than 12 million AIDS orphans in Africa.

Psychologists know that there is a heritable component to emotional capacity and that this affects the development of compassion among individuals. By fourteen months of age, identical twins (who share all genes) are more alike in how they react to an experimenter who pretends to painfully pinch her finger on a clipboard than are fraternal twins (who share only half their genes). But empathy also has a learned component, which has more to do with analytical skills. During the first years of life, within the context of early relationships with mothers and other committed caretakers, each individual learns to look at the world from someone else’s perspective.

And this is why I get so worried. Just because humans have evolved to be smart enough to chronicle our species’ histories, to speculate about its origins, and to figure out that we have about 30,000 genes in our genome is no reason to assume that evolution has come to a standstill. As gene frequencies change, natural selection acts on the outcome, the expression of those genes. No one doubts, for instance, that fish benefit from being able to see. Yet species reared in total darkness—as are the small, cave-dwelling characin of Mexico—fail to develop their visual capacity. Through evolutionary time, traits that are unexpressed are eventually lost. If populations of these fish are isolated in caves long enough, youngsters descended from those original populations will no longer be able to develop eyesight at all, even if reared in sunlight.

If human compassion develops only under particular rearing conditions, and if an increasing proportion of the species survives to breeding age without developing compassion, it won’t make any difference how useful this trait was among our ancestors. It will become like sight in cave-dwelling fish.

No doubt our descendants thousands of years from now (should our species survive) will still be bipedal, symbol-generating apes. Most likely they will be adept at using sophisticated technologies. But will they still be human in the way we, shaped by a long heritage of cooperative breeding, currently define ourselves?

An anthropologist with a long-standing interest in the natural relationships among males, females, and their offspring, Sarah Blaffer Hrdy began her research in the 1970s with a nine-year study of Hanuman langurs, a species that Indians regard as sacred. Her evolutionary perspective on families has resulted in two previous major essays for Natural History: “Daughters or Sons” (April 1988) and “Natural-Born Mothers” (December 1995). Hrdy is professor emerita of anthropology at the University of California, Davis, and the author of four books, including, most recently, Mother Nature: A History of Mothers, Infants, and Natural Selection (Pantheon Books, 1999).

Copyright © 2001 American Museum of Natural History

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