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Counterpoints in Science

Can This Pair Bond Be Saved?

Jerold Lowenstein

DNA fingerprinting has had an asteroidal impact on the human justice system, especially in cases of disputed parentage. It turns out that what's sauce for the human is also sauce for the gander, and the long-standing notion that many bird species have monogamous relationships has been turned upside down.

Before we had DNA fingerprinting, which was invented by Alec Jeffreys at the University of Leicester in 1985, individual identity in humans or animals was inferred by comparisons of blood groups and serum proteins. These tests had probabilities of Ornithologists missed the trysts going on right under their binoculars.
1-to-100 or 1-to-1000 of being the same for two individuals. In contrast, comparisons of minisatellite DNA can produce probabilities of one to a trillion, which is more than enough to distinguish every human on Earth from every other, except for identical twins. The DNA "fingerprint" is a mixture of the genetic patterns of the two parents, so parenthood can be established unequivocally rather than by racetrack-level odds. Usually, but not always, this means identifying the father.

Monogamy, originally defined as a long-term social and sexual relationship between one female and one male, is an unusual mating system in vertebrates. Males of most species irresponsibly take off right after insemination, often to look for other mating opportunities. The conspicuous exception among vertebrate phyla has traditionally been the birds, held up as models of fidelity and marital bliss, and of female-male cooperation in bringing up the young. Either male or female or both may build the nest, forage for food, or incubate the eggs. In many species of birds, the same male and female are seen socializing and procreating together each mating season until death do them part.

The shockeroo came about ten years ago when DNA fingerprinting was first applied to several "monogamous" species such as the indigo bunting and red-winged blackbird. Although careful field observations had failed to spot any deviation from a strict pair bond, the minisatellites told a terrible tale. One-third of the offspring of these closely bonded species had been fathered by males other than the mate--often a nearby neighbor!

Indeed, according to Luis Baptista at the California Academy of Sciences, DNA fingerprinting or blood protein studies have revealed that some 70-80 percent of socially monogamous songbirds have engaged in extramarital affairs and produced illegitimate offspring.

A female house sparrow can be a veritable hussy. Several observers have reported seeing female sparrows soliciting copulation with tails pointing upward and wings drooped down and quivering. The males line up like tomcats. A husband, returning to this disgraceful scene, drives off the rival males. He then massages her cloaca with his bill until she ejects the accumulated sperm, and then copulates with her himself.

These revelations stunned the hundreds of ornithologists who had logged in countless hours of birdwatching and somehow missed the crucial trysts (primly referred to as "extra-pair copulations" or EPCs) that must have been going on all the time right under their binoculars. This gross oversight demonstrates the truism that we tend to see what we expect to see and often screen out data that doesn't match expectations. It's hard to avoid the suspicion that the supposedly monogamous bird partnership was a projection of the idealized human nuclear family.

The finding of female infidelity in so many bird species was particularly disconcerting for the growing cadres of evolutionary theorists who try to explain in mathematical terms why it is that living organisms do the things they do, especially in the arenas of sex and reproduction. Female hanky-panky yanked the cornerstone out of their carefully erected house of cards.

From the theoretical point of view, it was expected that males would play the field and try to fertilize as many females as possible. In theory-speak, this is called "maximizing their fitness" by passing as many of their genes as possible into the next generation. This is what the vast majority of male animals do, as can readily be observed in virtually all domestic and wild species, not to mention our own. The theorists' problem, or so they thought, was to explain that notable exception, the birds. What accounts for a male giving up the joys of promiscuity and forming a pair bond with one female that lasts for many seasons, or for life? Why stick with one mate who can generally produce only one clutch of eggs per season when he could be enhancing his fitness with several different mates?

Well, the theorists labored and came up with an answer. It takes more time and energy to raise baby birds, they opined, than a single female parent can readily provide. Therefore, by settling down and pitching in, the papa bird increases the chances that his offspring will survive and perpetuate his genetic endowment. It doesn't do any good to father several broods if few or none of them survive to adulthood.

Female fitness, according to this theory, is maximized by having a single mate and sperm donor who will help around the nest and provide food and protection for the offspring. In this way, the female guarantees that her own genes will continue in the next generation. The DNA fingerprinting data, showing that females actually behave the way males were originally predicted to behave, caught the theorists with their hypotheses down. Female philandering was not only unexpected, it was hard to explain sociobiologically. In the world of evolutionary theory, every behavior must have some long-term survival value. What does the female gain from cheating on the pair bond? She doesn't end up with any more genetic offspring than she would have had with her mate and risks upsetting the partnership. What's in it for her, aside from the fun of a novel encounter?


Evolutionary theory is rather like psychoanalytic theory, in that its practitioners are particularly quick to retrofit explanations, even mutually contradictory ones, in response to newly observed behaviors. Some of the ideas put forth by different theorists for extra-pair paternity, according to Jeffrey M. Black in Partnership in Birds: the study of monogamy (Oxford University Press 1996), are: 1) The females are forced to copulate by horny males. 2) They are forced by males who threaten to kill their chicks. 3) They make sure this way that they get fertilized. 4) They trade food for sex. 5) They avoid retaliation from rejected males. 6) They prevent the sperm from being used to fertilize competing females. 7) They take multiple mates to avoid close inbreeding. This last notion assumes that the original mate may be a close relative. There is no good evidence to support any of these notions. To me, the fun factor makes as much sense as any of these labored speculations, but there aren't many formulae for fun in evolutionary algebra.

As might be expected, there is tremendous variety in the reproductive behavior of birds, and the past decade has seen an intense renewal of interest in the nature of their pair bonds. The DNA findings have forced ornithologists to distinguish between "social monogamy" and sexual monogamy. Some of these long-term field studies, many of them correlated with DNA fingerprinting, are reported in Black's book.

Geese and swans maintain the closest pair bonds, with almost no extra-pair conceptions. Barnacle geese fly from the high Arctic in summer to winter on coastal marshes in Scotland and England. Pairs maintain contact throughout the day, every day, for life. Iceland's whooper swans are known to mate exclusively within the pair. In contrast Australia's splendid fairy-wrens father only 30 percent of the offspring with their social partner.

"Pair bonds are not magical marriages," editor Jeffrey Black sums up, "but flexible associations that can potentially end any time another option arises." Even among the high-fidelity mute swans Clive Minton described one dramatic defection among the 100 pairs he watched in Staffordshire, England. After a prolonged battle, a usurper drove the territory-holding male away. The female, with her brood of four two-month-old cygnets, "sailed off down the stream with the new mate and family as if nothing happened." Just maximizing her fitness.

On the other hand, says Baptista, a female may stay with her mate even if he is not the best one available. He provides her with a territory in which to obtain food and raise young, while she may be enticing the guy-next-door, if he has better plumage or a better voice, to father her offspring.


Out of several thousand species of mammals, only five percent form monogamous pair bonds. Among our closest relatives, the apes, only the gibbons of Southeast Asia have been observed to have something like a nuclear family consisting of one female, one male, and their offspring, who share a territory and keep other gibbons out.

The gibbon story is strikingly similar to that of the birds. Starting early in this century, field workers described gibbon pairs as ideal marriages, mated for life, working industriously together to defend their territory and bring up the kids. Only recently has closer and more continuous observation revealed that there is trouble in this paradise, too.

Ryne Palombit, an animal behaviorist at the University of California at Davis, observed wild gibbons in Sumatra for six years. Of eleven pairs that he watched, two relationships were eliminated by the death of one mate, whereas five ended when either the male or female simply took off, in some cases to settle with a neighbor of the opposite sex who had recently lost its own mate through death or desertion.

One male left a mate who behaved antagonistically, making aggressive threats and refusing to groom_him. She treated her next spouse much better, but whether the departee found a happier alliance was not recorded. One male and one female left their mates for a time but ultimately returned to them. The Pickwickian injunction to "beware of vidders" was borne out by widowed gibbons, who almost invariably collected their new consort by breaking up a nearby pair, rather than going after the solitary "floaters" or the unattached young.

It's hard to resist the anthropomorphic reflection that these "monogamous" apes act in much the same way that human couples behave, as reported voluminously on "Oprah," in "Dear Abby," and in that long-running feature in the Ladies' Home Journal, "Can This Marriage be Saved?" Palombit concludes that "the complexities of social life in these animals extend beyond the narrow limits established by a rigid nuclear family concept."

Mating patterns among birds and primates are endlessly fascinating, and so far they refuse to be reduced to a formula in some theoretician's notebook. These creatures will keep right on maximizing their fitness in their own chosen ways, even if these ways shatter several generations' preconceptions about animal models of monogamy and fidelity.



Jerold M. Lowenstein is professor of medicine at the University of California at San Francisco and chairman of the Department of Nuclear Medicine at California Pacific Medical Center in San Francisco.

cover summer 2000

Winter 1998

Vol. 51:1