We have all seen it: the little horror at the supermarket till, alternately whining, sulking, arguing and throwing tantrums in an attempt to wheedle an extra bag of sweets out of its exasperated parent. Or was it, perhaps, your own offspring embarrassing you in public? Did you succumb for the sake of public decency? Or did you try to hold out despite the turned heads?
If this scene sounds all too familiar, take heart. The animal kingdom abounds with examples of clashes between parents and their offspring and what’s more, biologists have developed theories to explain these conflicts. Unfortunately, it is difficult to apply theories about animals to human parents and children because all human behaviour carries a weight of cultural, social and psychological baggage that clouds the issue. Nevertheless, some valuable insights into the human condition can be gained by examining conflicts between parents and infants in other species. Our closest living relatives, the nonhuman primates, inevitably offer some of the most valuable comparisons; but salutary lessons can be had from budgies, pelicans and opossum as well as baboons.
The pioneer of theories on conflict between animal parents and offspring is Robert Trivers, a biologist at the University of California at Santa Cruz – and himself a father of five. In a seminal paper published in 1974 he pointed out that, in species that reproduce sexually, there is an inherent conflict of interests between parents and their offspring because of differences in genetic relatedness.
Advertisement
In such species, each of the two parents contributes exactly half of each offspring’s genetic material. A parent thus shares 50 per cent of its genes with its offspring. Since a parent is equally related to each of its offspring, it will normally maximise its reproductive success by investing exactly the same amount of care and attention in each one. The individual offspring, however, take quite a different view: each is more closely ‘related’ to itself (100 per cent of its genes in common) than it is to any of its siblings (with whom it shares, at best, only 50 per cent of its genes).
Because of this, the infant would prefer the parents to lavish all their care and attention on itself, rather than share it out among its siblings, including those yet to be born. The conflicts that arise as the infant struggles to gain the maximum attention can occur at any time throughout the period of parental care, though these clashes are expected to be particularly fierce at the point when parents attempt to cease caring for their young.
Fighting in the womb
Conflicts, however, can begin amazingly early, almost as soon as offspring are conceived. In humans, for example, mother and fetus are engaged in a tussle over who should have hormonal control of the pregnancy as early as the seventh week of life. Morning sickness and the high blood pressure experienced by many expectant mothers can also be interpreted as signs of a disagreement between mother and offspring. In this case, the dispute is over what the mother should eat and how much oxygen the fetus should receive.
The story is very different in marsupials. Take the opossum. Its gestation period is only 12 to 13 days: the baby opossum is expelled long before it is in a position to disagree, at least hormonally, with its mother. This occurs because marsupial embryos are unable to prevent the mother’s immune system from attacking them. As far as the mother’s body is concerned, an embryo is foreign tissue, and must therefore be rejected. For the first two-thirds of the gestation period this is not a problem; the fetus develops inside the ‘shell membrane’, a maternal organ designed to keep out the lymphocyte cells that destroy foreign tissue. Once this membrane breaks down, the embryo is left without defences and has to leave the womb. Marsupial mothers would appear to have won this round of the conflict.
When it comes to placental mammals, though, the embryo has evolved the ability to fight back. It does this by masking certain molecules, called histocompat-ibility antigens, which trigger the mother’s immune system. In other words, the embryo effectively ‘disguises’ itself as maternal tissue so that the mother’s body has no reason to reject it. So, in placental mammals, it is the offspring who have the upper hand.
Irrespective of how the early stages of development are organised, things get worse once the infant is born or hatched. Soon after their entry into the world, offspring are arguing with their parents over the amount of food they should receive. Pelican chicks in the throes of such conflicts can even go into convulsions, literally throwing a fit in order to obtain extra food from their parents. They will fling themselves at their parents’ feet in a frenzy, beating (and even biting) their own wings and thrashing their heads back and forth. Given the chance, they will also attack any other chicks in the vicinity, driving them away.
It may not be very subtle, but this heavy-handed approach allows pelican chicks to solve two problems at once. First, they convey the message that withholding food could have quite serious consequences for the parents’ own reproductive success. Secondly, by driving their siblings away, they ensure there are no other competitors for the food they have worked so hard to obtain.
Budgerigar mothers stand for no such nonsense. They feed their chicks according to a strict rota, distributing food in proportion to their age and size. No amount of begging will persuade the female to forgo this discriminatory strategy. In contrast, the male is something of a soft touch. On the rare occasions that he feeds his offspring (he usually feeds only his mate), he gives food to those chicks that beg loudest and longest.
Not surprisingly, the rate of begging in budgie families rises dramatically when the male turns up with food. Quite why the male has never been able to evolve an effective strategy against manipulation to match that of his mate remains a mystery, though the infrequency with which he feeds the chicks is one likely reason because it means that selection will have had less opportunity to work.
Spotted flycatchers also have to be careful to avoid manipulation by their young. A study by Nick Davies of the University of Cambridge suggests that as the chicks grow, they continue to beg for food for as long as the parent is willing to feed them, even when they are perfectly capable of obtaining food for themselves. The chicks only start feeding themselves when their parents make begging unprofitable by forcing the young to chase them before they will surrender any food.
Why is it that parents have to be on their guard against this sort of manipulation? The answer seems to lie in the fact that parents and offspring never have perfect knowledge of each other: the parent never really knows how much care the infant needs, and the infant never knows how much care the parent is capable of providing.
Parents dare not take the risk that their offspring may be ‘crying wolf’ – it would obviously be disastrous if the offspring died as a result of insufficient care – so the odds are normally stacked in the offspring’s favour, at least in the short run. In the long run, though, there is only so much that parents can afford to do. Investing too much care in one infant leaves less time and resources for other offspring and may even place the parent’s own life in jeopardy: for example, a mother may draw too heavily on her fat reserves in order to continue providing milk for a demanding youngster. These considerations will soon generate a situation in which parent and offspring oscillate between alternating states of generosity and tough-mindedness.
Marc Hauser of Harvard University looked at precisely this problem in vervet monkeys in Kenya’s Amboseli National Park. He began by using game theory to model the strategies that vervet mothers and infants could adopt. Game theory is a way of analysing animal behaviour by first envisaging the members of a population as playing games against each other in which they employ various strategies, and then assessing the ‘payoffs’ (the value of a strategy in terms of Darwinian fitness) that result. In many cases, one individual’s payoff from a particular strategy will depend on strategies other individuals are using. Game theory models are thus highly appropriate to the study of social behaviour, where interactions such as these are frequently observed.
Hauser’s model suggested that infants should adopt the strategy of being ‘deceitful’ – that is, exaggerating their actual needs – in order to extract more care. However, should the mother become ‘sceptical’ and refuse to administer the amount of care that the infant demands, the infant should drop its ‘deceitful’ behaviour and revert to being ‘truthful’. The model suggests that there will be a continuous cycling of strategies, whereby first the infant, and then the mother, gets wise to what the other is doing.
Dangers of deceit
At certain points in the cycle, however, the infants’ strategy of deceit may backfire with a vengeance. When infants become truthful in response to their mother getting wise to their exaggerated demands, there will be a period during which mothers become vulnerable to the cry-wolf syndrome. They may well fail to recognise that their infants are being truthful about their needs, and continue to behave as though the infants are still crying wolf.
Hauser’s observations of vervet monkeys bore out this aspect of the model. One particular infant continually demanded care from its mother until she eventually began to ignore it. One day the infant ran into trouble following its mother up a tree, and began to scream for help. The mother took no notice and continued on her way – at which point the infant fell out of the tree. It died from its injuries a few days later.
Parent-offspring conflict doesn’t always have to end in tragedy, however. Our own work on nursing behaviour in gelada baboons in Ethiopia has shown that conflict between mothers and infants can sometimes be part of a ‘training’ process designed to produce a more harmonious relationship between the pair. The source of conflict in this case is not the amount of investment (in the form of milk) that the infant receives, but the timing of that investment.
During the first two months of life, mother geladas allow their infants to suckle and cling to their chest for much of the time. As the infants grow bigger, however, their presence on the mother’s chest becomes ever more of an encumbrance – especially when the mother is feeding. The gelada’s unusual feeding habits are to blame for this: the baboon’s diet consists almost entirely of grass, and they feed by squatting on the ground and harvesting grass blades immediately in front of them. Clearly, the efficiency of this mode of foraging is going to suffer if a female has to reach around a squirming infant before she can get her hands on some food.
The ideal solution, from the mother’s point of view, is for the infant to be out of contact when she is feeding, and suckling when she is engaged in an activity such as resting or grooming where a clinging infant is not a hindrance. This arrangement suits both parties. The infant is happy because the amount of time it spends on the nipple does not change, but is merely rescheduled, while the mother is happy because she is able to forage with maximum efficiency – an extremely important consideration for nursing mothers, for whom the extra feeding time required to fuel lactation takes a big chunk out of their overall time budget.
To arrive at this happy state of affairs, however, the mother has to train her infant to make contact only at the appropriate times. She achieves this by rejecting her infant whenever it attempts to make contact while she is feeding, and ignoring the inevitable consequences. Probably because they assume that the mother is trying to reduce the quantity of milk, gelada infants take a dim view of this at first and react in time-honoured fashion – by throwing tantrums. Occasionally, infants will even manage to bounce off the back of a nearby male in the course of a tantrum – apparently in the knowledge that few mothers will risk the mistreatment of their infants at the hands of an irascible male. It seems that, like human toddlers, they soon learn that parents are less likely to ignore them if they make a public scene.
Generally, though, the mothers resolutely ignore the entreaties of their young until they learn that resistance is useless. From then on, they attempt to suckle only when it is convenient to the mother and soon learn to anticipate periods when the mother will be amenable to providing a feed. An infant that is off playing with its friends will run back to its mother the moment it sees one of her regular grooming partners approaching – often arriving ahead of the prospective groomer to sit waiting, poised to grab a teat the moment the mother stops eating.
When mothers give in
There is a maternal learning curve in all this, too. First-time gelada mothers are much more easily panicked into letting the baby back on the nipple when it whines and grizzles or throws a tantrum. Montserrat Gomendio of the University of Cambridge showed that, in captive rhesus macaques, subordinate mothers are much more likely to allow their infants onto the nipple than higher-ranking ones because they want to keep them out of harm’s way, fearing that the infants will be punished by other group members. And with good reason, as Dario Maestipieri, now at Duke University in Durham, North Carolina, was able to show. He found that the infants of low-ranking macaque mothers were much more likely to be maltreated by other group members if the mother was preoccupied with grooming another animal rather than keeping an eye on her baby.
Jeanne Altmann of the University of Chicago has shown that a similar training process takes place among the yellow baboons at Amboseli. Yellow baboon mothers do not deter their infants from suckling freely until they are in their fourth month of life. The rate of development is similar in gelada and yellow baboons, so this cannot account for the difference in timing. Instead, it seems likely that contrasting diets and feeding styles are responsible.
Yellow baboons eat a great deal of fruit and generally have a more varied diet than gelada baboons, and they typically remain standing while they feed. A clinging infant is unlikely to interfere with its mother’s feeding behaviour until it has reached quite an appreciable size. Yellow baboon mothers therefore do not need to restructure suckling schedules quite as early as the gelada.
Monkey mothers and infants living in captivity show much lower levels of conflict than either gelada or yellow baboons. This is because the mother does not have to spend such a large proportion of her day feeding and has more time to devote to the care of her infant. Nevertheless, conflicts do occur. Gomendio found that with captive rhesus macaques, behavioural conflict between mothers and infants intensified dramatically during the mating season.
At first glance, this seemed to be a classic case of the mother wishing to start investing in her next offspring, and the current infant objecting to termination of investment in itself. However, Gomendio found that despite the high levels of rejection the infants were experiencing, there was no change in the frequency with which they gained access to the nipple. Instead, she showed that the situation was analogous to that of the gelada.
During the mating season, female rhesus macaques shift all their attention to sexual interactions with males, and aggressive interactions with other females. Females therefore are unable to devote as much time as usual to their infants. In addition, the presence of a suckling infant is as much an encumbrance to a mating macaque as it is to a feeding gelada. Rhesus mothers therefore employ the same regime of negative reinforcement as the gelada to train their infants to keep out of the way when they are busy with other things.
Conflicts between parents and offspring are a natural and widely occurring phenomenon in the animal world – a consequence of the fact that animals have evolved so that their offspring try to gain just a bit more care and attention than they are entitled to. The only difference in the human case is that human children learn faster and are more skilled at social manipulation, and so can bring more powerful social pressures to bear. They soon learn that most parents will do anything rather than let their children scream in public. So if you find yourself being emotionally blackmailed into buying an extra large bar of chocolate or yet another computer game, breath deeply and just remember that it’s all part of the game of life.
Louise Barrett and Robin Dunbar study primate behaviour in the Department of Anthropology at University College London.
