How have our views of primate behaviour changed over the past few decades?
Right from the beginning, many people made the implicit patriarchal assumption that the world ran in accordance with Victorian ideals, with sexually ardent males in pursuit of coy females. So once scientists began to look at primate behaviour from female as well as male perspectives, this led to a real transformation. Some have read feminist politics into the transformation, but as I see it, if selection pressures on half the species were ignored, and then subsequently taken into account, this simply means better science being done.
For once we realised how much individual variation exists, we looked for sources of variation in female as well as male reproductive success, and that led fieldworkers to theorise about the strategies females engage in to increase their reproductive success and inclusive fitness. This sets off a chain reaction: once we give females strategies, then in order to understand males we also need to know how males respond to female strategies, and then in turn to consider female counter-strategies to male counter-strategies.
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Was it your work on infanticide in langurs that set you thinking this way?
Infanticide is a classic paradigm for evolutionary interactions between the sexes. The langur monkeys I studied in India live in breeding groups with a single male, and every 27 months on average you would have males from an all-male band come in from outside and take over the troop. When that happens, one of the usurpers would attempt to eliminate offspring sired by his predecessor. Essentially, they were eliminating the last mate choice the mother made, and also increasing their own probability of breeding with her 鈥� because a bereaved mother will resume ovulating sooner than she would have done if she had continued to lactate.
You see this happening, and you think, how are females responding? Females in that situation have a range of options, none of them terribly good. Among them is mating with a range of males to confuse paternity. Males then have to counter their counter-strategies. Today, evolutionary theorists like William Rice at the University of California, Santa Cruz, use the term 鈥渟exually antagonistic co-evolution鈥� to describe this kind of dynamic process.
The idea of those counter-strategies will be a real shock to many people, especially the notion that females might benefit from having quite a lot of partners who feel that they may or may not be the father鈥�
When I published The Woman That Never Evolved, I expanded the argument that females might try to mate with a number of males to confuse paternity, and that this might apply in humans as well. The idea was not well received. For example, Don Symons, who wrote the key work The Evolution of Human Sexuality, said in an essay called 鈥淎nother woman that never existed鈥� that this simply could not have been part of our evolutionary heritage. His reasoning was that a human female needs investment from a husband to provide for her and help her raise her extremely costly infant.
Of course I agree that human females need a lot of help, but I envision mothers as resourceful opportunists who elicit help from a range of different parties. Many aspects of women鈥檚 personalities are about just this 鈥� eliciting support. But Symons was assuming that that kind of help was only going to come from a husband certain of his paternity, otherwise, he believed, no male would invest. As far as I was concerned, this was just another patriarchal presumption. For by then I already knew that so long as care is not too costly and exclusive, males help rear even infants who are not their own.
In baboons, for example, females mate with a number of males, and males they have mated with will look out for that female鈥檚 offspring. New data from Robert Seyfarth and Dorothy Cheney鈥檚 field site at Mikumi in South Africa indicates that 41 per cent of all infants born there are killed by males, but these killers are males the mother did not mate with. Ryne Palombit鈥檚 鈥減lay-back鈥� experiments from that population reveal that when a strange male is harassing infants, some resident males respond to maternal calls for help if the plea comes from a female they have mated with. Certainty of paternity then is not the sine qua non for 鈥減aternal鈥� assistance.
What about humans?
Studies of hunter-gatherers suggest that meat brought in by male hunters is shared among the group rather than channelled to their mates or offspring. Kristen Hawkes at the University of Utah has proposed that men share in order to enhance prestige which in turn 鈥� by appealing to women 鈥� improves their love life. Along similar lines, Polly Wiessner also of the University of Utah, who studied the !Kung of Botswana and foragers in New Guinea, thinks that hunters are sharing meat in order to influence the political composition of the group, since kin and others helpful for rearing their offspring tend to cluster around successful hunters.
I agree, and believe that such sharing is integral to a species that evolved (as I believe humans did) as a cooperative breeder. The motives of these hunters are very different from those assumed by Irv DeVore of Harvard University and the late Sherwood Washburn, when they laid out their 鈥渕an the hunter鈥� model. Like Darwin, they assumed that fathers hunted to provide for their highly dependent offspring, and that the men who were the smartest and the most capable with tools were the best hunters who provided for their infants better. And they thought that鈥檚 how humans evolved really big brains and so forth. It all depended on a one-man woman waiting for her mate to bring food back. It鈥檚 an inherently appealing paradigm that just will not go away, even as the evidence for it is dismantled.
So are humans also busily confusing paternity?
Some are, some aren鈥檛. I often see claims on the back of books about evolutionary psychology that 10 per cent of human offspring are sired by someone other than the husband. But that kind of global statistic is misleading. That high proportion applies in some populations, say inner cities where mothers are pursuing a strategy of mating with a number of males because job opportunities for men are awful and no one man in that community can reliably support her offspring. High rates of misattributed paternity are also found in Amazonian societies like the Canela or the Ache, where men who go off hunting or fishing may or may not come back with anything to eat. Or else, a woman鈥檚 husband might die, or decamp. Under such circumstances, mothers cannot afford to have just one mate.
Fortunately for children in those societies, mothers often have more than one, and use strategies of what I call 鈥減olyandrous motherhood鈥�. Here mothers line up multiple 鈥減ossible fathers鈥� and sequential 鈥渇athers鈥�, facilitated by a widely accepted folk belief in 鈥減artible paternity鈥�. Every man a woman had sex with in the 10 or so months preceding a birth is considered a progenitor, who is expected to provide both the pregnant women and her progeny with protein-rich gifts.
What exactly is this partible paternity?
The Ache, Canela, Bari, Yanamamo 鈥� people from different language groups from a vast Amazonian area 鈥� believe that fetuses are built up over time, like the lustre on pearls, by repeated applications of semen. According to anthropologist Kim Hill of the University of New Mexico, the Ache have different words to refer to 鈥渢he man who put it in鈥�, 鈥渢he one who mixed it鈥� and so forth, and men who provide either sex or meat to the mother are considered to have contributed to the creation of a child.
All these 鈥済odfathers鈥� are expected to help provide for the child. And as Penn State anthropologist Steve Beckerman has shown for the Bari of Venezuela, a husband plus one secondary father correlate with the best chances of offspring survival. This is why a Canela woman who suspects she is pregnant will try to seduce the group鈥檚 best hunters and fishermen. I like to imagine some white-haired grandmother dreaming up this story. It鈥檚 so obviously beneficial to the survival of her grandchildren.
How common is this?
More common than I had realised before starting to research Mother Nature. It was really eye-opening, and I am now starting to catalogue cases of polyandrous motherhood The pattern crops up not just in much of lowland South America, but if we are talking about informal polyandry (rather than institutionalised polyandrous marriage), it is very widespread.
You have to keep in mind opposing forces, however, and another pattern which is very widespread in societies with patriarchal histories: enforced chastity for women who are constantly monitored and among whom female adulterers are severely punished.
Is this kind of motherhood connected with the evolution of concealed ovulation?
I call it 鈥渁bsence of advertised ovulation鈥� and it鈥檚 very widespread. Only 27 of 175 or so species of primates exhibit conspicuous ovulation, the famous red sexual swellings that chimpanzees, Barbary macaques and baboons flaunt at mid-cycle.
Sexual swellings puzzled Darwin. But he was not thinking in terms of females soliciting multiple males. The behaviour that goes with them in the wild, frantic solicitations of multiple partners, it鈥檚 obvious females are attempting to draw as many males as they can into the web of possible paternity. And since a lot of these species tend to be infanticidal, there鈥檚 method to the seeming madness of mating with multiple males.
But the pattern differs for species with and without conspicuously advertised oestrus. The species that advertise ovulation with swellings live in multi-male units. All the males that the females could mate with are there in the group so it pays females to mate as efficiently as possible. For females trying to make a living, having to go around looking for males to mate with is a nuisance. How can she feed? So she compresses all the hubbub into a space of a few days and makes the males come compete for her. All very efficient.
Why are langurs so different?
In langurs there is usually just one adult male in the troop, although other males living in all-male bands are roving around on the outskirts of these breeding troops. A female cannot know when she is likely to encounter stray males, so she keeps her options open by not signalling ovulation physically. Absence of advertised oestrus permits a female the flexibility to solicit males when an opportunity arises, even when she is already pregnant.
So if you are a female in a multi-male group where you know everybody, it is better to compress your mating into discrete mating times. But if you might run into strangers, then concealed ovulation has the advantage. Either way, very few of the males females have mated with are going to be certain that they are not the father, and in primates, a male cannot afford to harm an offspring that is possibly his.
Is infanticide the only reason to solicit multiple partners?
Oh no, there are other reasons as well, such as avoiding inbreeding. Among langurs, for example, females in troops where the same male has been there year after year are more likely to solicit outside males than females in troops with new males. In the Langurs of Abu, I proposed that flexible and opportunistic solicitations were a way to avoid inbreeding. Research by Patricia Adair Gowaty at the Institute of Ecology at the University of Georgia and by Jeanne Zeh at the University of Utah suggests that in other animals 鈥減romiscuous鈥� females are increasing the chances of getting a genetically compatible mate, and so forth.
Given all this dubious fatherhood, our ancestresses were going to need a wide range of helpers to help rear their young. Who fits the bill?
I am increasingly convinced that in contrast to other apes, humans evolved as co-operative breeders. It takes about 13 million kilocalories to rear a human infant from birth through to nutritional independence, and hunter-gatherer women don鈥檛 peak in their skill at gathering food until they are quite old. Mothers needed help from allomothers 鈥� group members other than the mother. I agree with Kristen Hawkes that grandmothers were important for raising children. After all, post-reproductive females are an especially dedicated, skilled, motivated type of allomother. But I also think other group members 鈥� aunts, older siblings, brothers and former lovers 鈥� helped at various points in the child鈥檚 long period of dependency. In the last few years, empirical support has accumulated to the point that we can say that when group members other than the mother and father are on hand to help provide for offspring, survival rates zoom up.
It looks as if there is a battle between the quality mode, in which the female insists on rearing quality offspring, and the quantity mode, in which the male insists on making many offspring. Is there a way out?
One of my favourite studies of all in science is the work of Rice and Brett Holland with drosophila. The males are very polygynous and females are promiscuous, although I would prefer to call them 鈥減olyandrous maters鈥� since 鈥減romiscuous鈥� is just a word to describe a female having more sex than someone else thinks she should. Anyway, drosophila males increase their own reproductive success by releasing toxic molecules in their seminal fluid along with the sperm, a potion that increases the chance that their sperm will inseminate the female. But these molecules are so toxic that even though they increase the chance that the female will produce young soon, over cumulative matings the poisons significantly shorten her life.
Rice and Holland鈥檚 brilliant if draconian experiment was to impose monogamy: for 44 generations each male could breed with only one female and each female with only one male. Guess what happened? After 44 generations, the sperm ceased to be toxic. Monogamous male drosophila were forced into reinventing the Talmudic injunction 鈥淟ove your wife as yourself and honour her more.鈥� After all, her reproductive success is his reproductive success.
Should we try that with humans?
That experiment wouldn鈥檛 get past human subject review boards since you can鈥檛 go around imposing chastity on future generations who haven鈥檛 given their consent! But Symons proposed a 鈥渢hought experiment鈥�, described in Steven Pinker鈥檚 The Blank Slate. If you put a man on a desert island with one woman, his wife, and their descendants dispersed and lived with just their own wife each, what would happen after many generations?
Pinker assumed that the castaways would be bored out of their gourds, and intellectually devolve into blobs. But I don鈥檛 think so, not if you take into account that humans are parents as well as fornicators. Generations of enforced monogamy would produce incredibly nurturing hyper-parents, who would also evolve to be frighteningly competitive towards other parents. That is, it wouldn鈥檛 be all evolution towards boring sweetness and light, and certainly not towards becoming mindless blobs. The writer David Lodge made a similar point about novelists: 鈥淟iterature is mostly about having sex and not much about having children. Life is the other way around.鈥� Early evolutionists were too focused on copulation at the expense of realising just how hard it was for our ancestors to keep offspring alive.
But in fact you have also been concerned about parents who are anything but hyper-nurturing?
Yes. I am very worried about the future impact of current patterns of child-rearing. In the past, infants who were not in constant contact with someone else failed to survive. Today, children live in walled houses, are fed from baby bottles and are not at constant risk from predation, so children can experience all manner of neglect and still survive to breed.
I believe that this poses a real threat to the perpetuation of traits we view as quintessentially human, such as being able to put oneself cognitively and emotionally in someone else鈥檚 shoes. There is a heritable basis to empathy, which is why identical twins are more similar in this respect than non-identical twins. But there is also an important developmental component. Empathy emerges around three years of life in the course of interaction between the baby and its caretakers. A child who grows up in a very caring environment will tend to be much more caring, but worldwide, higher proportions of children are surviving rearing regimens that are far less caring than those it took to ensure survival among children in the past. The genetic basis for empathy will be there, but never have a chance to fully develop. Unfortunately, once lost, these traits can be hard to retrieve in subsequent generations.
That鈥檚 very frightening鈥�
It has long been known that securely attached mothers produce securely attached offspring. Many psychologists assumed this was due to heritability of particular personality types. But as University of Delaware psychologist Mary Dozier has demonstrated, children adopted by very warm and responsive foster mothers who themselves were very securely attached to their caretakers, were more likely to become securely attached themselves, compared to children cared for by foster mothers who had been themselves insecurely attached.
There were exceptions 鈥� children who had been abused or seriously neglected. But here鈥檚 the point: we are not just talking about genetic predispositions. If a child had had even moderately reasonable care up to the point of assignment to the super-nurturing mother, they came out very secure.
This also means 鈥� and this is the scary part 鈥� that children who grow up emotionally neglected are unlikely to produce offspring whose human potential for empathy is fully expressed. Genetic traits not selected are invisible to selection. A hundred generations down the line, I wonder how good we humans will be at empathy? How caring? For me, the obvious message is that super-nurturing caretakers should be identified, cherished and enlisted in rearing future generations. Instead, even if such nurturers find themselves working at a day-care centre, it only means they can expect to be overworked and poorly paid.
