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UNTIL death us do part. With these words Christianity enshrines the idea that
humans are a monogamous species. So why do more than a third of all marriages in
Britain and half of those in the US end in divorce? And how come as many as 15
per cent of children are fathered by a male who is not their registered father?
Some people see this as a sign of the times: a breakdown in family values, the
disintegration of society, or a modern disease that requires everything,
including relationships, to be “new and improved”.

Recently, however, biologists have come up with another explanation. We are
finding that monogamy is not a fixed and immutable instinct, hard-wired into
some animals’ brains, as we previously thought. Even creatures once considered
as paragons of fidelity will indulge in a fling if the situation is right.

Take the South American marmoset and tamarin monkeys. Both are usually
monogamous in the wild, with males largely responsible for bringing up the
young. But in some cases, males engage in roving polygamy, hitching up with a
succession of females. “Divorce” rates can be as high as a third of all pairs in
the population during any one year. This radical change in behaviour is often
prompted by an excess of males, usually because of high female mortality. With
females in short supply, males who cannot get a mate become
“helpers-at-the-nest”, willing to assist with the rearing of offspring that are
not their own. The presence of a helper increases the chances that a breeding
male will desert his partner and go searching for another female because he will
be able to breed again sooner than if he waited for his current mate to come
back into breeding condition. The helper gets his payoff next time the female
comes into oestrus, when he mates with her. And the females seem indifferent to
their mate’s behaviour: so long as they have a male to help with rearing the
offspring, they don’t seem to mind too much who he is.

The key to understanding what is going on is to look at the benefits of the
altered mating strategy. My mathematical models of this behaviour show that,
under the right environmental conditions breeding males who are powerful enough
to pursue this kind of roving strategy can gain up to twice as many offspring as
they would by remaining in a normal monogamous relationship. Females fare no
better or worse since either way they reach their optimum reproductive
potential, and the helpers make the best of a bad situation. In this case, the
new behaviour is a response to a change in circumstances and benefits some of
the males. But even without external changes, it may be in the interests of
monogamists—both male and female—to adopt a more flexible approach.
Indeed, human behaviour is by no means unique. The animal world, it turns out,
is full of examples of cuckoldry, cheating and even divorce, by supposedly
lifelong mates as they try to overcome what I call the monogamist’s dilemma.

Breaking the rules

Monogamy is relatively rare in nature. Only about 5 per cent of mammals are
monogamous, with primates and dogs favouring the practice more than most. But
there is one group of animals for which monogamy is the rule. Around 90 per cent
of bird species pair, at least for a given breeding season. On the surface it
looks like the wedded bliss conjured up by the ubiquitous photos of bride and
groom. But a decade or so ago, that illusion was blown away when the new
technology of DNA fingerprinting revealed that as many as a fifth of the eggs
produced by monogamous female birds had not been sired by their regular
partners. Many male birds were busily feeding offspring that were not their
own.

What was going on? Behavioural ecologists who had previously focused on
cooperation as the driving force behind monogamy (see “Only you”) had to revise
their views about mating strategies. They began to see the flip side of the
coin: that alongside cooperation comes the inevitable risk of exploitation. A
monogamous male can never be sure that he is the father of his partner’s young.
In cooperative systems, it always pays some individuals to opt for the free-ride
strategy by leaving their allies (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 his mate and risk being cuckolded,
or to abandon family life and risk losing his own offspring because their mother
cannot feed them by herself.

He 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 the DNA analysis had
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.

Perhaps the best known example is provided by the humble dunnock, a small and
undistinguished looking British sparrow. Nick Davies and his colleagues at
Cambridge University have used DNA fingerprinting to show that male dunnocks
weigh up very accurately the effort they put into bringing food back to the nest
against the number of nestlings they have sired. And how do they achieve this
remarkable feat? By the very simple trick of 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 male next door.

Humans are also highly suspicious of extramarital relationships, a fact
attested to by the frequency with which separated husbands are now resorting to
DNA fingerprinting to avoid paying former wives for the upkeep of their
children. 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
10 and 13 per cent of all conceptions in Britain arise from matings with
non-pair males. They based their estimate on self-reports of the frequency of
double matings—matings with both the normal partner and another male
within five days of each other—around the time of ovulation.

Both men and women seem, at a subconscious level at least, to realise that
paternity may be in doubt. We see this in the comments that people make about
newborn babies. Martin Daly and Sandra Wilson at McMaster University, found that
mothers and their relatives are disproportionately more likely to refer to
similarities between the baby’s features and the man’s than to the
mother’s— despite the fact that one newborn baby looks pretty much like
any other.

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 cooperation rather than coercion:
too aggressive a policing strategy may well drive the female away. In
Californian chuckwalla lizards, for example, very aggressive territorial males
achieve fewer matings because they scare females away. Barbara Smuts, of the
University of Michigan, Ann Arbor, has shown that overly aggressive male baboons
suffer the same fate: females spurn their attentions in favour of socially more
skilful males.

By the same token, the male’s response to suspicions of cuckoldry should not
necessarily be outrage. Although a male risks rearing children unrelated to him,
he should continue to treat all his partner’s children as his own so 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 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 must pay to reproduce at all.

It is easy to see what a male gets from playing away from home, but what does
the female gain from acquiescing in an extra-pair relationship? Current thinking
makes two possibilities the frontrunners. The first can be described as hedging
bets. 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.
She also wants a mate with good genes, a quality which 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—those that do are usually swamped by suitors. She may 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 finds them.

An alternative explanation for a female’s interest in extra-pair males 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 mathematical modelling 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. Analysis of international data by Daly and
Wilson shows that the vast majority of spousal murders in humans are triggered
by actual or suspected infidelity. Both men and women often use aggression to
try to prevent a mate abandoning them, but sometimes males play their hand too
heavily.

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

Clear off

Maria Sandell of Lund University, studied this experimentally in European
starlings. During the egg-laying period, strange 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 more aggressive towards the rival. More importantly, Sandell was
able to show that females who were more aggressive towards their rivals were
more likely to retain a monogamous relationship with their male throughout the
breeding season than less aggressive females.

Any monogamous partnership is built on tension. Flexible behaviour allows
individuals to exploit every opportunity to pursue their needs. So we should not
be surprised to see that nature is full of partnerships being dissolved as new
and better opportunities come along. Indeed, researchers are finding that
“divorce” is common, even among birds that supposedly pair for life, like swans.
Estimates of pair-bond dissolution vary enormously, both across species and,
within species, across populations. Over half of all pairs of Belgian great
tits, for example, get divorced. André Dhondt, now at Cornell University,
Ithaca, New York state, found that not only do females often instigate divorce,
but they usually benefit from doing so by subsequently producing more offspring.
The luckless males, however, do not always fare so well.

Failure to rear offspring is one common cause of avian divorce. Indeed,
failure to have children is also one of the highest risk factors for divorce in
humans. However, there are as many other routes to divorce in avian society as
there are in the human case. Lewis Oring of the University of Nevada, Reno,
studies the killdeer, a North American plover. He has found
“home-wreckers”—individuals that muscle in on another pair and drive the
same-sex member out so that they can bond with its mate. Bob Furness of the
University of Glasgow has seen similar behaviour in great skuas, a seabird whose
ferocious reputation is attested to by the fact that attempts to oust a member
of an established pair may result in its death.

If there is a message in all this, it must surely be that there are no simple
rules that apply to all of the species all of the time. There are some key
general principles that apply universally, but patterns of monogamy, divorce and
polygamy vary both between and within species in response to local ecological
and demographic conditions. But it is the availability of alternatives that
makes shifts of strategy possible. Animals, every bit as much as humans, make
choices about whom to pair with and for how long, 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.

CONVENTIONAL wisdom has it that male birds are loyal and faithful because the
business of feeding nestlings is so demanding that it takes two to rear the
clutch successfully. Cooperation is therefore the best way of ensuring
reproductive success.

By contrast, most mammals have a lengthy gestation followed by lactation,
which leaves males on the sidelines. With little to contribute to the rearing
process, they tend to opt for polygamy in one form or another.

Male mammals are only monogamous under a limited number of conditions. One is
when females are so widely dispersed that a male would find it difficult to
defend more than one at a time. In this case, he may do well to stick with one
female to make sure that no other males mate with her when she does come into
oestrus. The dik-dik, a diminutive African antelope, is one species that seems
to live by this rule.

However, many species are monogamous even when males could in principle
defend several females. In these cases, it turns out that the male provides a
service for the female. By investing in her and his young, the male gains more
offspring in a lifetime than he does by pursuing the alternative strategy of
roving polygamy.

In South American marmoset and tamarin monkeys, this service amounts to full
responsibility for everything to do with childcare, except lactation. As a
result, females manage to produce twins twice a year—if they had to do all
the work alone, it is unlikely that they could do better than a single infant
once a year. So, males who become monogamous and share the workload can expect
to obtain around four times as many offspring as males who abandon their mates
in favour of serial polygamy. A polygamous male would have to locate and mate
with at least four times as many females as a monogamous one, so it pays to be
monogamous.

Another form of service that the male can provide is to act as a “hired gun”
to protect the female from predators or other infanticidal males. Steve Emlen,
at Cornell University, has argued that female bee-eaters form pair bonds with
males to reduce the levels of harassment from the many males that hang around
their communal nest sites.

Much the same idea has been used to explain why gorilla and perhaps
chimpanzee females associate with individual powerful males. Indeed, Carel van
Schaik, at Duke University, has even argued that the use of males as hired guns
to reduce the risks of infanticide has been a crucial driving force in the
evolution of primate social structures.

As for humans, monogamy may have been gone hand in hand with the evolution of
large brains. Pair bonding could have ensured that women got enough food to
raise their big-brained, slow-growing and highly vulnerable offspring to
adulthood. Our ancestors probably opted for some form of monogamy when they
began eating meat and hunting.