How Many Friends Does One Person Need? (28 page)

What on earth is going on? Behavioural ecologists, who had previously focused on co-operation as the driving force behind monogamy, had to revise their views about mating strategies. They began to see the flip side of the coin: that together with co-operation comes the inevitable risk of exploitation. Monogamous males can never be sure that they are the father of their partner’s young. In all co-operative systems, it always pays some individuals to opt for the free-rider strategy by leaving their friends – in this case, literally – holding the baby. That way, they gain all the benefits without having to pay the costs. The monogamist’s dilemma is whether to stay with your mate and risk being cuckolded, or to abandon family life and risk losing the offspring you have just sired because their mother cannot rear them on her own.

Males would like to have it all. And in evolutionary terms that means developing sneaky strategies to mate with new females, while finding ways to avoid wasting energy bringing up the offspring of other males. Once DNA analysis revealed the extent of extra-pair mating, researchers began to see the mating game for what it was and anti-cuckoldry strategies also started to be noticed. It also works the other way round, of course. Perhaps the best-known example is provided by the humble dunnock, the small and undistinguished-looking British hedge sparrow. Nick Davies and his colleagues at Cambridge University have shown that male dunnocks adjust the effort they put into bringing food back to the nest exactly in proportion to the number of nestlings they have sired (as determined by DNA fingerprinting). And how do they achieve this remarkable feat? By the very simple trick of
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estimating how much time the female was out of their sight during the egg-laying period. That, it turns out, is a very good estimate of the likelihood that she was engaging in a little fling in the bushes with the chap next door.

Humans are also highly suspicious of extra-marital relationships, a fact attested to by the frequency with which separated husbands are now resorting to DNA fingerprinting to avoid paying their former wives for the upkeep of children who aren’t in fact theirs. And it seems they may be justified. A few years ago, Robin Baker and Mark Bellis, then both at the University of Manchester, calculated that between ten and thirteen per cent of all conceptions in the UK arose from matings with non-pair men. They based their estimate on self-reports of the frequency of double matings – matings with both the normal partner and another man within five days of each other – at around the time of ovulation.

In some cultures, males attempt to sequester their wives in harems where the opportunities for infidelity are greatly reduced, or persuade them to wear blandly uniform clothing supposedly for religious reasons. Such behaviour is just a form of mate-guarding, no different to the numerous examples seen in many animal species. Where society favours less formally structured relationships, men and women seem, at a subconscious level at least, to realise that paternity can be an issue. That’s one reason why, as I mentioned in Chapter 8, in-laws make so much fuss about newborn babies looking like their father. It looks suspiciously like an attempt to persuade the husband that the baby really is his and so encourage him to invest in the baby.

However, careful analyses of the evolutionary costs and
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benefits of rearing another man’s offspring suggest that a male’s response to suspicions of cuckoldry should not necessarily be outrage. Although a male risks rearing children unrelated to him, he would do best in the long run if he treated all his partner’s children as his own, as long as doing so allows him to maintain a satisfactory relationship with her and thereby gain access to most of her future reproduction. Being too inquisitive may backfire by raising too many doubts in his own mind or by causing his partner to desert him in favour of a kinder rival. Rearing a few offspring sired by another male may simply be the cost some males are obliged to bear in order to reproduce at all. It seems that Freud might have underestimated the benefits of repression.

It is easy to see what a monogamous male gets from playing away from home. But it takes two to tango, so what does the female gain from acquiescing in an extra-pair relationship? Current evolutionary thinking on this emphasises two possibilities. The first can be described as bet-hedging. Ideally the female would like a male who will invest in her offspring: a man with a bulging wallet, perhaps, or a robin with a large breeding territory. But she also wants a mate with good genes, something she might assess by looking at his tail if she is a peahen, or by the symmetry of his features if she is a woman. But females usually have to trade one component off against another because the world is imperfect and few males come with high ratings on all dimensions – and those that do are usually swamped by suitors. So perhaps she could
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try to get the best of both worlds by teaming up with a good provider and allowing him most – but not all – of her conceptions, while allocating the rest to better-quality mates as and when she can.

An alternative explanation for females’ interest in extra-pair matings is that it is a way of forcing their pair-male to be more attentive. Magnus Enquist and his colleagues at Stockholm University have used a simple mathematical model to show that females can play one male off against another in this way to prevent their pair-male straying in search of other females with whom to mate. But, once again, there is a fine line to tread. Martin Daly and Margo Wilson have shown, using data from all around the world, that the vast majority of spousal murders in humans are triggered by actual or suspected infidelity. Both men and women often use aggression as coercion to try to prevent a mate abandoning them, but sometimes males overplay their hand too heavily.

Even so, intra-sexual jealousy seems to be the first line of defence for maintaining the pair-bond in many species. In titis, one of the many small monogamous South American monkeys, females are quite intolerant of the approach of strange females, and will drive them away. And I have observed similar behaviour during fieldwork on the small monogamous African antelope known as the klipspringer.

Maria Sandell of Lund University, Sweden, studied this experimentally in European starlings. During the egg-laying period, stranger females were placed in small cages near to the nest-box used by an established wild pair. Males offered the opportunity of a second female showed considerable interest, but their females were rather aggres-
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sive towards the rival. More importantly, Sandell was able to show that females who were more aggressive towards the rival were more likely to retain a monogamous relationship with their male throughout the breeding season than were less aggressive females.

Nonetheless, evolutionary interests suggest that individuals should be open to better reproductive opportunities that happen to come their way. So we should not be surprised to see partnerships being dissolved as new and better opportunities come along. Researchers are finding that ‘divorce’ is common even among birds like swans that supposedly pair for life. Estimates of pair-bond dis-solution vary enormously, both across species and, within species, across populations. André Dhondt, now at Cornell University, found that over half of all pairs of Belgian great tits, for example, get divorced. Not only did the females often instigate divorce, but they usually benefited by subsequently producing more offspring when they did. The males, however, did not always fare so well.

Failure to rear offspring is one common cause of avian divorce. Failure to have children is also one of the highest risk factors for divorce in humans, and not just among Muslims. (Under Islamic law, a wife’s infertility is an appropriate reason for divorcing her and sending her back to her parents. Infidelity by a wife – but not by a husband – may even be punishable by death.) However, there are as many other routes to divorce in avian society as there are among humans. Lewis Oring of the University of Nevada, Reno, studied killdeer, a North American plover, and observed ‘home-wreckers’ – individuals that muscle in on another pair and drive the same-sex member out so that they can take over its mate. Bob Furness
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of the University of Glasgow has seen similar behaviour in great skuas, a sea bird whose ferocious reputation is richly attested to by the fact that its attempts to oust a member of an established pair may sometimes result in the luckless victim’s death.

If there is a message in all this, it must surely be that there are no simple rules that apply to all species all of the time. As is invariably the case in biology, there are some key general principles that apply universally, but the patterns of monogamy, divorce and polygamy vary both between and within species in response to the way these principles work themselves out in the local ecological and demographic conditions. Any animal with a decent-sized brain – and that most obviously includes humans – has its brain in order to tweak its behaviour to take advantage of the momentary circumstances it happens to find itself in. It is the availability of alternatives that makes shifts of behavioural strategy possible.

Animals, every bit as much as humans, make choices about whom to pair with and how long for, and those decisions are influenced in large part by whether they will do better by staying with the current partner, by moving from one partner to another or by playing a more subtle kind of game.

Humans are caught in the same bind as any other monogamous species. The male wants to monopolise his mate’s future reproductive output, but he has to tread a careful line. Mating is ultimately a game of co-operation not coercion: too aggressive a policing strategy may well put the female off and drive her away. In Californian chuckwalla lizards, for example, very aggressive territorial males achieve fewer matings because they scare females
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away from their territories. And Barbara Smuts, of the University of Michigan, has shown that overly aggressive male baboons suffer the same fate: females spurn their attentions in favour of socially more skilful males.

A great deal of fuss has been made in the media about oxytocin, the so-called ‘love hormone’ that characterises monogamous species. In fact, oxytocin seems to have this effect only in females. In males, a related but rather different neuro-endocrine called vasopressin seems to be the active ingredient in these monogamous species. Vasopressin seems to play an important role in modu-lating male behaviour in monogamous species. When inserted into their brains, it makes male rodents more tolerant of females and young, more willing to engage in huddling behaviour and less aggressive. Inevitably, people have begun to wonder if it plays a similar role in humans. Given the difficulty we have in deciding whether humans are monogamous or promiscuous, maybe the issue is not so much that all human males should be high on the vasopressin dimension (and hence monogamous), but rather that there are differences among males that might correlate with promiscuous behaviour.

Hasse Walum, of the Karolinska Institute in Stockholm, and his colleagues used a large sample of 552 Swedish twins to look at the relationship between vasopressin receptor genes and marital stability in men. They checked out a number of genes in the region that codes for the vasopressin receptor. They found that one particular gene
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site, RS3, varied significantly as a function of the man’s score on a partner-bonding scale that measured their commitment to relationships. And of the eleven different gene variants that occurred at this site, one in particular (allele 334) showed much the strongest effect.

Men who had one or two copies of the 334 allele (in other words, a copy inherited from one or both parents) scored lower on the partner-bonding scale than men who had two copies of any of the other ten alleles. They were also more likely to be living with, rather than married to, their partner – something suggestive of reduced commitment. One-third (thirty-three per cent) of double-334 men reported that they had experienced marital stress in the past year, against just sixteen per cent of single-copy 334 men and fifteen per cent of males who lacked the 334 allele. And all this despite the fact that all the men in the sample had been living with their partner in a stable relationship for at least five years and had at least one child with them.

In the Swedish sample, about four per cent of the men had two copies of the 334 allele and thirty-six per cent had one copy, leaving almost two-thirds of men having no copies and being a good bet for a devoted, monogamous partner. So, although the number of complete bas-tards (those with a double dose of the offending gene) seems to be very small, around a third of men seem to be a risky bet. A similar ratio was found in a very large survey carried out in Quebec by Daniel Pérusse: he found that around one third of the men in Quebec were habitually promiscuous, with about two-thirds being habitually monogamous (at least while they were in a steady relationship).
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In the Quebec case, I was able to show that while promiscuous men would, as individuals, have sired more offspring over a lifetime than monogamous men (based on the frequency of copulation and the probability of conception occurring on any given copulation), the relative difference in siring rates between the two types of men exactly balanced their respective frequencies in the population. This suggests that monogamy versus promiscuity is a balanced evolutionary polymorphism, with the proportions of the two strategies held in approximate balance across the generations by the costs and benefits of pursuing the different strategies.

Although it’s tempting to interpret these findings in terms of vasopressin being a male ‘gene for monogamy’, it almost certainly isn’t – not least because the genetics of life are rarely so simple. Behaviour is often the outcome of predispositions laid down by the genes, rather than an outcome of the genes themselves. So it was interesting to see, in a recent study carried out by Dominic Johnson (now at the University of Edinburgh) and his colleagues, that males who had the RS3 gene were inclined to react aggressively when put in a threatening situation. It seemed that the RS3 gene simply causes men to fly off the handle quicker in response to something as simple as frustration. So men with the 334 allele are not genetically promiscuous: rather, they just don’t think before they act.