Sunday, July 01, 2001

The Dark Continent of Sexual Strategies

The Myth of Monogamy: Fidelity and Infidelity in Animals and People

By: Geoffrey Miller Ph.D.

rev_v3n3miller_2

There is more to monogamy than meets the eye. Beneath the placid surface of social monogamy—the long-term cooperative breeding relationships characteristic of birds and humans—swirl the deep waters of infidelity. The Myth of Monogamy looks at the chaotic, convective currents between the two layers. It reviews surprising recent evidence of pervasive infidelity among socially monogamous birds and the evolutionary psychology of human mating. As popular science, The Myth of Monogamy is an enviable success, covering new research clearly and concisely, and reminding us that the mating strategies of other species are more complex (just as our own are often simpler) than we care to admit.

The authors, David P. Barash and Judith Eve Lipton, have been monogamously married since 1977, producing together two children and four previous books, including Making Sense of Sex. Barash has a Ph.D. degree in zoology from University of Wisconsin and is professor of psychology at the University of Washington in Seattle. His dozen books address topics such as marmot behavior, nuclear war, human violence, and the pleasures of outdoor activities—topics unified by his evolutionary perspective on life. Barash was an early, ardent advocate of a Darwinian perspective on human psychology. Lipton is a psychiatrist specializing in women’s mental health at a Seattle hospital and a social activist. 

Their teamwork is apparent in the evenhandedness with which they view male and female sexual strategies as equally well adapted, subtle, and important. They also share an interest in the psychological aspects of the nuclear arms race—arguably a fruitful model for the psychology of marriage, with mutual destruction, frosty détente, or mutual disarmament and reciprocal trade as the only realistic options. They seem to have been disarmingly candid with each other about their thoughts and feelings as exemplars of male and female psychology. One of the pleasures of the book is trying to imagine how they might have argued through some of the thornier issues. In a recent New York Times interview, journalist David Rakoff asked Barash, “How has all of this [scientific insight] played itself out in your own marriage?” to which Barash responded “The overt biologizing of our inclinations can be very clinical and, in that sense, rather helpful.”

His droll reply identifies a great advantage of talking about humans within a biological framework. The terms used to describe animal mating behavior sail smoothly between the Scylla of euphemism and the Charybdis of profanity. This enables the reader to set aside moralistic reactions to loaded language and to consider people as just another sexually reproducing species with a distinct repertoire of behaviors and preferences. Instead of “extramarital affair,” they say “extra-pair copulation”; instead of “jealousy,” “mate-guarding.”  The clinical language strips the romantic mystique away from both fidelity and infidelity, so both can be assessed more objectively as sexual strategies with certain costs, benefits, and risks. Not that the biological terminology is without its charm, as when Barash and Lip-ton pepper their writing with journal article titles such as “DNA Fingerprinting Reveals Multiple Paternity in Families of Great and Blue Tits,” “Density-Dependent Extra-Pair Copulations in the Swallow,” and “Old, Colorful Male Yellowhammers Benefit from Extra-Pair Copulations.”

BRAD AND JULIE AND JULIETTE AND JOHNNY

Despite its provocative title, The Myth of Monogamy reaches a modest, well-supported conclusion: Monogamy is a fragile and flawed compromise, a relationship balanced on a finer strategic knife edge than most biologists had realized. The book’s most distinctive feature is its sensitivity to the inescapable co-evolution between males and females, the running battle of the sexes in which every temporary advantage for one sex is eroded by counteradaptation by the other. 

Monogamy is a fragile and flawed compromise, a relationship balanced on a finer strategic knife edge than most biologists had realized.

The book’s news is mostly about birds, and mostly about the genetic benefits of infidelity for females. It was never a surprise to Darwinians that males should be willing to have extra-pair sex. The more lovers a male has, the more babies, and the more copies of his genes make it into the next generation. So Darwinians expected males to be ardent, promiscuous, and indiscriminate, spreading their genes into any available fertile females. Since females bear much heavier costs of gestating and nurturing each offspring, they were expected to be coy, choosy, faithful, and naturally monogamous. This view immediately raised a knotty question: In socially monogamous species, why would any female ever be willing to have an affair? The sexual math doesn’t seem to add up: Unless females have affairs sometimes, there is no possibility of males having affairs, so selection could not favor males who wasted any effort on unrequited courtship outside their own monogamous relationships. 

Barash and Lipton answer this by considering the downside of monogamy from the female’s point of view. The trouble is that good males are hard to find. Every female wants to attract the highest-quality male she can, to get the best genes for her offspring. Among most mammals, this is not a problem: All local females can have sex with the most attractive local male, and ignore all the other males. But given social monogamy, as in most birds, the situation is different. Social monogamy implies that males help raise their offspring, and this costly paternal investment gives males an incentive to be sexually choosy. In fact, under perfect monogamy, with no divorce and no infidelity, males should be just as choosy as females. There would be mutual choice. The highest-quality male would pair up with the highest-quality female, leaving the second-highest-quality pair no option but to settle for each other. 

In fact, under perfect monogamy, with no divorce and no infidelity, males should be just as choosy as females. There would be mutual choice.

For example, without monogamy, both Julia Roberts and Juliette Binoche could enjoy Brad Pitt, as any normal female mammals would; but with monogamy, Brad might choose to invest all his energies in Julia, leaving Juliette no choice but to settle for Johnny Depp. Here’s the point of infidelity: If Juliette can have a secret liaison with Brad, she can get his superior genes, while retaining Depp’s devotion. This is precisely the strategy that seems to have evolved among socially monogamous female birds and primates. 

BETTER GENES BY HAVING AFFAIRS

What exactly are females getting from these affairs? In the last decade, there has been a revolution in thinking about female sexuality, from a focus on their getting male resources to getting male genes. The old story was that a female chose the highest-status male for his resources, his territory, and his protection, and once satisfied with a good match, would stay sexually faithful and produce his offspring. The only incentive for infidelity would be a sort of prostitution benefit; perhaps females somehow gained extra resources by having affairs, if their male lovers gave “nuptial gifts” of food or allowed the females to forage on their territory. Such sex-for-food exchanges are fairly common among insects, but appear not to explain much infidelity in birds or primates. 

The book’s key conclusion, in my view, is that many socially monogamous female animals, including humans and most birds, have adaptations for covert, short-term mating to get better genes for their offspring than their steady partner can deliver. In this way, they can combine the resource benefits of social monogamy with the genetic benefits of exercising female choice for the highest-fitness males. This leads to rampant infidelity whenever females can get away with it and to the development of a distinctive short-term sexual psychology attuned to male genetic quality. 

Throughout most of the twentieth century, biologists resisted the idea that females could choose males for genetic quality, whether in long-term relationships or brief affairs. Evolutionary geneticists such as R. A. Fisher predicted that populations would converge onto the highest-fitness variant (or allele) of each gene very quickly, so there should no longer be any variation in fitness-related genes. Thus, if all males are equal in genetic quality at evolutionary equilibrium, there would be no incentive for females to choose males on the basis of good genes, whether as monogamous partners or illicit lovers. 

In the last few decades, however, genetic data have shown that most species, most of the time, are not at evolutionary equilibrium. Genetic variation is common, and is often associated with variation in survival success or reproductive success. This massive genetic variation in fitness-related traits is caused by two factors: co-evolutionary changes in the other species (especially fast-breeding parasites) to which each species is adapting, and new harmful mutations continually eroding fitness from each generation to the next. These two factors are enough to create wide variation in the genetic quality of individuals in most populations, fostering incentives for mate choice in both short-term affairs and long-term relationships. 

This point about variation in genetic quality should not be confused with the DNA fingerprinting methods that are emphasized throughout the book as the best evidence for infidelity. DNA fingerprinting has been pivotal in showing that most socially monogamous birds are not sexually monogamous. About 10 to 40 percent of offspring have DNA that could not have come from the mother’s partner. However, the genetic variation used in DNA fingerprinting is mostly from highly variable regions of the genome that do not get expressed as important traits. 

THE TROUBLE WITH HUMANS

Humans are the most birdlike of primates: not only two-legged, but socially monogamous. The book explains how we can understand ourselves by considering distantly related species that share similar reproductive challenges, rather than closely related apes with very different mating systems. Our sexual psychology may be much more similar to that of communal-nesting, socially monogamous birds than to that of our close relatives, the promiscuous chimpanzees or harem-forming gorillas. This is why the evidence on infidelity among birds is so informative about human sexuality.

Our sexual psychology may be much more similar to that of communal-nesting, socially monogamous birds than to that of our close relatives, the promiscuous chimpanzees or harem-forming gorillas.

One problem with the book’s treatment of humans, however, is that the reader may get the impression that monogamous relationships are entirely unnatural—mere cultural constructs. It is fair enough for the book to show the differences between the cultural norm of monogamy and the biological reality of pervasive infidelity among humans, but I would welcome more attention to our adaptations for sustaining successful sexual and parental relationships. These pair-bonding adaptations in humans range from the hormonal (oxytocin) through the emotional (long-term companionate love) to the cognitive (effective anticipation of each other’s needs). 

Although Barash and Lipton rightly challenge the view that humans are instinctively monogamous unless tempted by the devil, in the end they fail to undermine the view that—compared to almost all other primates and mammals—humans are unusually good at forming and sustaining socially monogamous, cooperatively breeding relationships. Nor do the authors attend enough to research by David Buss and others concerning our very effective adaptations for deterring infidelity: mate-guarding, sexual jealousy, the threat of spousal homicide, and the like. 

The chapters on humans also have a methodological flaw: They too often follow cultural anthropology’s tendency to assume that everyone within a culture agrees on what is normal, and that there are no strategic conflicts within cultures concerning sex.

The chapters on humans also have a methodological flaw: They too often follow cultural anthropology’s tendency to assume that everyone within a culture agrees on what is normal, and that there are no strategic conflicts within cultures concerning sex. For example, the authors claim: “In ancient India, sex by a married man with a prostitute or slave woman wasn’t adultery, unless she was someone’s property, in which case it was an offense against the owner.”  Does this mean that ancient Indian men never tried to be discreet in visiting prostitutes? Did such visits never provoke jealous marital arguments? Did a wife never object to a man buying a new slave girl? Many such anthropological generalizations have no basis in quantitative research. They come from a few talkative “informants” who are self-anointed experts on the local norms. 

The problem of generalization within cultures is amplified when the authors generalize across cultures. What does it mean to say that 39 percent of the 185 societies from a cultural database “not merely tolerated but actually approved extramarital sexual liaisons”? Who is tolerating or approving? All husbands, all wives, and all their children, kin, in-laws, and friends? Does a philandering husband in such cultures never come home to his wife’s icy stares, sexual rejection, or determination to be unfaithful herself? Does he never suffer social pressure from her brothers, uncles, and male friends to behave better? 

There is a startling inconsistency of scientific method here. In discussing birds, the authors highlight the strategic intricacies of mating, the sexual conflicts of interest, the tough trade-offs each individual faces, and the ecological and demographic variables that affect mating patterns even within a species. But when it comes to humans, it is as if human minds soak up the dominant cultural norms and implement them without any tension, argument, rebellion, variation, or strategic subtlety. 

Modern evolutionary psychology cautions against these generalizations about what is “permitted” or “acceptable” in any given culture. A focus on individual sexual strategies, and sexual conflict between individuals, should heighten our sensitivity to the sexual conflict endemic within any society and the conflicting ideologies that individuals will use to advance their interests. 

IMPLICATIONS FOR SCIENCE AND SOCIETY

This book should lead to clinically useful insights for marriage counselors and family therapists, and to a better understanding of social emotions such as lust, love, companionate attachment, jealousy, and betrayal. It should lead psychiatrists to view in a more skeptical light the alleged clinical syndrome of “sex addiction” (as claimed by ultra-high-status males such as actor Michael Douglas and musician Mick Jagger). It should also lead to a better understanding of the ways in which certain disorders affect sexual behavior. For example, that mania often leads to extra-pair copulations in people with bipolar depression may help explain the persistence of this disorder over evolutionary time. Likewise, the hair-trigger jealousy and sense of betrayal characteristic of borderline personality disorder may be a window on the evolutionary psychology of infidelity. 

This book should lead to clinically useful insights for marriage counselors and family therapists, and to a better understanding of social emotions such as lust, love, companionate attachment, jealousy, and betrayal.

The book also points up some methodological pitfalls of doing correlational studies without considering the role of general fitness in behavior. The bird evidence shows that the male bird who has affairs usually has higher mate value and better genes than the one who does not—because he can attract more females. Conversely, the female bird who has affairs usually has lower mate value and worse genes than the one who does not—because she could not attract a high-quality male in the first place as her primary partner. The same pattern may hold in humans. If one studied co-morbidity (how often the same two or more disorders are found together in one person), one might discover that female but not male infidelity has a high correlation with illness, infertility, low intelligence, neuroticism, and many other markers of low fitness.

From this, a psychiatrist untutored in sexual strategy theory might conclude— wrongly—that infidelity is a maladaptive aberration for females but not for males. The reality might be that they are all doing the best they can, given their fitness. But without explicit consideration of variation in fitness and how it affects an individual’s strategy, it is easy to be misled by correlations in any area of brain and behavior research. The result is that scientists may posit a disorder where there is none—especially when a behavior associated with lower fitness (like female infidelity) also happens to deviate from a social norm. 

Biological discoveries about infidelity have essential social implications, but the book’s discussion of them, in the final chapter, is weak. Like most scientists, the authors examine the human implications of their work at just two levels: government social policy and individual lifestyle. Why? There are additional levels worth considering. How should one give marital advice to friends or family in the light of this research? Should corporations promote family-friendly environments by minimizing the temptations of extra-pair copulations with co-workers? How should the research inform marriage counseling, sex education, media portrayals of relationships, bioethics, and other issues that lie midway between national policy and individual choice? 

Because they are ambivalent about promoting monogamy as a social norm, Barash and Lipton skirt such questions. They could have left the choice to the reader, however, by saying: If you want to promote monogamy for social and familial stability, here are some things that might help; on the other hand, if you want to promote the eugenic benefits and emotional thrills of infidelity, then here’s what to do. Despite their credentials as social activists, Barash and Lipton seem willing to accept the sexual status quo, rather than challenging it in the name of more fulfilling lives for both men and women— for example, by legalizing polygyny, or by re-introducing the ancient European custom of annual festival weeks that permit infidelity. Like most psychologists since Freud, they favor individual adaptation to current cultural norms, rather than the radical redesign of society to better fit our natural inclinations. 

Despite their credentials as social activists, Barash and Lipton seem willing to accept the sexual status quo, rather than challenging it in the name of more fulfilling lives for both men and women— for example, by legalizing polygyny, or by re-introducing the ancient European custom of annual festival weeks that permit infidelity.

In general, though, their book’s shortcomings are minor and its strengths important and unusual. Barash and Lipton skillfully convey the strategic complexity of relations between the sexes and research that is unraveling the diverse reproductive strategies that have evolved in socially monogamous birds and humans. Their writing is engaging and their biology is surefooted. If The Myth of Monogamy does not qualify as a classic of the genre, that is only because, dealing as it must with a fast-changing field, its content is likely to be superseded in a few years, as new discoveries help us map the dark continent of sexual strategies.

 

 EXCERPT

From The Myth of Monogamy: Fidelity and Infidelity in Animals and People by David P. Barash and Judith Eve Lipton. ©2001 by David P. Barash and Judith Eve Lipton. Reprinted with permission of Henry Holt and Company. 

This much is clear: Females are inclined to have EPCs [extra-pair copulations] with males who have good genes. And as we have seen, ‘good genes’ can include many things: being sufficiently different from the female in question (but not too different), being genetically complementary in other ways, or carrying health-related genes. But this isn’t all. If certain characteristics (symmetry, bright plumage) indicate good genes and if, as a result, females are at an evolutionary advantage if they prefer these characteristics, then the stage is set for yet another wrinkle in the EPC saga: Females can benefit by preferring those males whose only virtue is that they are preferred by other females! Such a preference might well begin with traits that are “genuine,” such as symmetry or bright plumage, but as the pioneering evolutionary geneticist R. A. Fisher pointed out decades ago, it could quickly develop a life of its own…. 

For example, in a species of sandfly, females evince clear preference as to mates. In one experiment, females were denied the opportunity to exercise choice and were forced to mate with either preferred males or males who would otherwise be shunned. There was no impact of paternity on the overall health or viability of their offspring. But the offspring of preferred males were themselves preferred, just as shunned males produced sons who were shunned in turn. 

When it comes to EPCs, females of many species are especially likely to mate with males who are more attractive than their partner. You can almost hear the females— whether already mated or not—spotting the animal equivalent of a movie star and sighing to themselves: “I want to have his kids.” If so, the reason appears to be that, at an unconscious level, they can hear the echoes of other females saying the same thing about their future offspring, thereby promising a larger number of grandchildren for the besotted, starstruck, would-be mother…who is now a candidate for one or more extra-pair copulations with the lucky hunk. 

The converse also holds: Make a male less attractive, and his mate is more likely to look elsewhere for male genes. There is, for example, a small, strikingly colored socially monogamous Euroasian bird known as a bluethroat. Males have—not surprisingly— bright-blue throats; female throats are white. When researchers from the University of Oslo, in Norway, used dye to diminish the blueness of their mates’ throats, female bluethroats were more likely to engage in EPCs. (It is also interesting that the de-blued males apparently perceived somehow that they were less attractive than before, perhaps because of changes in their mates’ behavior, since they increased their mate-guarding activities... although to no avail.)



About Cerebrum

 
Bill Glovin, editor
Carolyn Asbury, Ph.D., consultant

Scientific Advisory Board
Joseph T. Coyle, M.D., Harvard Medical School
Kay Redfield Jamison, Ph.D., The Johns Hopkins University School of Medicine
Pierre J. Magistretti, M.D., Ph.D., University of Lausanne Medical School and Hospital
Robert Malenka, M.D., Ph.D., Stanford University School of Medicine
Bruce S. McEwen, Ph.D., The Rockefeller University
Donald Price, M.D., The Johns Hopkins University School of Medicine

Do you have a comment or question about something you've read in CerebrumContact Cerebrum Now.