Games Primates Play: An Undercover Investigation of the Evolution and Economics of Human Relationships

by Dario Maestripieri

  In an incomplete or aborted greeting, one male winks at another one and starts walking toward him, but when the other turns the other way and does nothing, the first male stops and goes back to where he was. Sometimes the two males approach each other, but a second before grabbing each other’s testicles they change their minds, then quickly turn around and retrace their steps. It’s as if one or both of them thought at the very last second that this intimate exchange wasn’t such a good idea after all, or freaked out about how the other one might react. Another researcher who has studied greetings between male baboons, University of Michigan primatologist Barbara Smuts, discovered that of over six hundred greetings she observed, about half were incomplete because one male, or both, pulled away before completing the exchange.4 The interruption of the sequence could occur at any time, ranging from right at the beginning, when one baboon initially glanced at the other, to almost at the end, when his hand was beginning to touch the other’s testicles. Observing the interaction on slow-motion videotapes, Smuts discovered that during the course of a greeting two baboons monitor each other and respond to the subtlest glances and shifts in movement with split-second timing. Any sign of hesitation in the other partner can be a reason for terminating the greeting before it’s complete.

  When two baboons fondle each other’s genitalia, they take a huge risk. Each baboon could quickly and easily terminate the other’s reproductive career for good by ripping his testicles off. Thus, letting another baboon fondle one’s testicles shows a great deal of trust in the other’s good intentions. On the other hand, by getting so close to another male and attempting to touch his testicles, a male exposes himself to a high risk of aggression. A single bite inflicted with a male baboon’s sharp canines could scar someone for life. Again, initiating a greeting requires a great deal of trust that the other individual will not respond aggressively to this potentially dangerous violation of privacy. Greetings work only if both males are equally committed to being friendly. When friendly feelings are not fully reciprocated—for example, when a low-ranking male tries to befriend the alpha male but the alpha is uninterested—greetings are attempted but aborted.

  Occasionally greetings end in a fight. Smuts reported that about 7 percent of the greetings she observed ended in threats, chases, or physical aggression. Pairs of very close friends show the most intense greetings—those in which both the penis and the testicles are fondled for a few seconds—and their greetings are never incomplete. When relationships are good, it doesn’t really matter if one partner ranks higher than the other. Generally, low-ranking males initiate greetings about as often as high-ranking males do. A low-ranking male may use a greeting to gather information on the dominant’s willingness to tolerate and support him. A high-ranking male may use a greeting to communicate his willingness to accept a low-ranking male’s presence in his group and his availability as a potential ally. The two partners in the cooperative relationship frequently assess each other’s commitment to it—testing the strength of their bond—by imposing on each other. What makes the greeting work as a bond-testing mechanism is the risk associated with it—and therefore the potential cost that each individual is willing to pay to maintain the relationship. By taking the risk and tolerating the imposition, male baboons demonstrate how much they value their relationship. Let’s now explore in more detail why this is the case.

  The Logic of Bond-Testing and the Handicap Principle

  The importance of bond-testing was highlighted in “The Testing of a Bond,” a paper published in 1977 by an Israeli evolutionary biologist, Amotz Zahavi, who presented some novel and controversial ideas about cooperation and communication.5 As an evolutionary biologist, Zahavi reasoned that cooperative relationships between individuals who are not genetically related to one another are intrinsically less stable than those involving family members. Two unrelated individuals, as we know, may form a cooperative relationship because they have shared interests and want to jointly pursue goals that would be difficult or impossible to accomplish without a partner, such as having children. Zahavi recognized, however, that the circumstances that hold a cooperative relationship together can change quickly and unpredictably. Therefore, he emphasized, it is important to frequently test the strength of the bond and assess the partner’s commitment in order to decide whether to continue investing or bail out.

  Take human romantic relationships. The most direct way for romantic partners to assess their mutual commitment to the relationship is simply to ask each other all the time, “Do you love me?” “Are you sure you love me?” or “Are you sure you want to be with me forever?” Couples in love do this all the time, as they should, but unfortunately this is not the most reliable of methods for assessing commitment (and for animals, it’s not an option at all). People can be insincere, or even clueless, about their feelings and future behavior. Zahavi’s original idea was that the most reliable way to assess how much a relationship is worth is to assess its market value, that is, how much someone is willing to pay for it. Your boss at work can tell you that you are a valuable employee and praise your work constantly, but the best indicator of how valuable you are to your boss is the salary he or she is willing to pay you. Words are cheap, but money isn’t.

  When money is not involved, the price one is willing to pay for a commodity can be counted in a different currency. For animals, the most meaningful currency is fitness: the ability to survive and reproduce. This is the currency that natural selection does business with. To assess the value to an animal of a commodity (such as food, a mate, or a relationship with an alliance partner), one has to measure the extent to which the animal is willing to risk its survival or future reproduction to obtain or keep that commodity. According to Zahavi, “The only way to obtain reliable information about another’s commitment is to impose on that other—to behave in ways that are detrimental to him or her.” Zahavi believes that the information about commitment obtained with this bond-testing mechanism is reliable because only partners who are truly committed will accept the imposition. By gradually escalating the imposition and determining the point at which the partner will terminate the interaction, one can obtain precise information about the other’s commitment to the relationship and current willingness to invest in it. A male baboon who wants to know exactly how much his alliance partner values their relationship can continue holding his partner’s testicle until he gets smacked in the head or bitten. The probability of getting a negative reaction increases exponentially with time, so being able to prolong the ritual for even one second is a significant accomplishment that bespeaks the strength of the commitment.

  The idea that the strength of a social bond can be tested by imposing a cost on the partner is one application of the more general theory known as the Handicap Principle, which Zahavi first presented in 1975 and expanded and refined in subsequent years.6 The HP was developed to explain the existence of honest or unreliable information in animal communication, but it could be applied to many other phenomena as well, including, as we’ll see later, many aspects of human behavior. The main idea of the HP is that a cheap signal is easy to fake and anyone can do it, while expensive signals require resources that only superior individuals possess. Therefore, expensive signals convey honest information about the quality of the individuals who are able to use them.

  Zahavi purportedly had the idea for the HP while attempting to explain to a student why peacocks have giant and elaborate tails and why peahens prefer to mate with males with the longest, heaviest, and most cumbersome tails: if large tails were cheap to produce, then all males would have them, regardless of age, size, strength, or health. But a large tail ain’t cheap and may actually be detrimental to the male’s survival: it’s expensive to produce and can hamper the peacock’s mobility, potentially reducing his ability to escape a predator. Strong, healthy males can afford huge tails, while weak and sick males can’t. In Zahavi’s terms, the peacock’s tail is a handicap. So why would a male want to take on such a handicap? Per
haps simply to show the female that he can. The peacock is self-handicapping to show the peahen how good he is. The bigger the handicap, the better the male.

  Thus, according to the HP, individuals signal their quality by displaying traits that are detrimental to themselves. Signals with handicaps are inherently honest owing to their cost; females trust males who display such signals and find them attractive as mating partners. Of course, peacocks who handicap themselves with a large and expensive tail don’t do it by conscious choice; sexual selection, not conscious thinking, is responsible for the evolution of large tails. The males with the genes for such tails are more attractive to females, reproduce more than other males, and therefore leave more copies of their genes in the population.

  The peacock’s tail is an example of a physical handicap, but handicaps can be behavioral as well. Behaviorally, a handicap can entail taking risks that may reduce one’s probability of survival. One classic example of a behavioral handicap is the stotting behavior displayed by African gazelles when confronted by a predator, such as a lion. When gazelles spot a lion, some of them start jumping up and down in front of him instead of fleeing as fast as they can. Why do these animals waste time and energy on behavior that could jeopardize their life? Zahavi’s answer is that stotting is a handicap and that some gazelles take it on to communicate how strong and fast they are. They are telling the lion that they would be difficult to catch and therefore a waste of time. The lion would be better off chasing the easier prey—the other gazelles that are trying to get away as quickly as they can. The assumption here is that lions sometimes do chase the stotting gazelles, or at least did so in the past when stotting behavior first evolved. The gazelles who cheated and stotted even though they were not fit enough to do it paid with their lives, and their genes were not passed on to the next generation. Over evolutionary time, the genes for cheating were wiped out by natural selection while the genes for honest stotting spread in the population. (Note: This example is an oversimplification to illustrate how natural selection works. In fact, specific single genes for “honesty” or “deception” don’t exist, and behavioral traits are often controlled by multiple genes interacting in complex manners.)

  Another, less well-known potential example of behavioral handicapping in the animal world involves the bizarre behavior of adult male baboons holding an infant in the middle of a fight.7 Imagine this scene. Two male baboons are about to have a fight: they threaten each other by staring each other down and ominously displaying their canines. All of a sudden, one of the males grabs a nearby infant—sometimes forcibly removing it from its mother’s arms—then continues to threaten his opponent, holding the infant in his arms. Why does he do this? Is he telling the other guy that he is a father and begging for mercy? Is he threatening to harm the other’s son? Is he trying to use the infant as a shield? The HP suggests another explanation: fighting while holding an infant in one’s arms is clearly a handicap, so by grabbing and holding an infant, a male wants to tell his opponent that he is so strong that he can beat him in combat even with an infant in his arms. It’s the primate equivalent of: “I can beat you up even with my hands tied behind my back.”

  For all three examples—the peacock’s tail, the gazelles’ stotting behavior, and the baboons’ infant holding—there are other possible explanations, though it has proven difficult for researchers to establish which of them are correct. But the explanation provided by the HP is interesting and makes sense; until it is tested and unequivocally discarded with appropriate data, it is as viable as any of the others.

  According to Zahavi, the HP explains not only costly and extravagant morphological traits and risky and bizarre behaviors in animals but also many general social phenomena, including altruism and nepotism. Zahavi argues that when individuals behave altruistically they are not really trying to help others. Instead, they handicap themselves to advertise their own quality and resources. Self-handicapping for the purpose of advertisement works even better when money or resources are not donated to others but simply wasted, as in the human phenomenon of conspicuous consumption. Rich people like to waste their money on luxurious yachts or fancy cars, not because they need them but simply to show off. University of New Mexico evolutionary psychologist Geoffrey Miller has written a book, called Spent: Sex, Evolution, and Consumer Behavior, in which he argues that many forms of wasteful spending in contemporary human societies are manifestations of the Handicap Principle.8 Wealthy men throw their money away to make themselves attractive to potential mates, and both men and women waste money on luxury goods to gain social status with their peers. Again, there are other explanations for acts of altruism such as wealthy people’s donations to charities, some of which I discussed in Chapter 5. And many economists would probably object to the notion that the HP and its role in mate attraction fully explain consumer behavior in capitalistic societies. However, I suspect that economists—at least those at my parent institution—would be generally sympathetic to the reasoning at the basis of this principle. The HP paints a view of the world in which living organisms are fundamentally rational and selfish creatures and their social interactions are governed by the rules of the market and the advertising business. The HP explains the natural world using the principles of capitalism.9

  Although there are many similarities in the cost-benefit analyses used by economists and evolutionary biologists, as well as an increasing awareness that these disciplines show a great deal of convergence in their general principles, back in the 1970s, when the HP was first proposed, this kind of reasoning was radical in evolutionary biology. By proposing economic cost-benefit analyses of animal signals, Amotz Zahavi was way ahead of his time. And as it may be easily imagined, his ideas were met with a lot of skepticism and resistance before they were accepted, or even taken seriously, by other evolutionary biologists. In fact, he continues to fight this battle after thirty-five years now. Whether he has won or lost the battle depends on who you talk to, but one thing is certain: he has managed to get a lot of people’s attention in the process. His personal story and the vicissitudes of the HP nicely illustrate, in many ways, how the process of scientific research works and some of the dynamics between researchers I discussed in Chapter 5.

  At the time of this writing, Amotz Zahavi is eighty-two years old and an emeritus professor of zoology at the University of Tel Aviv in Israel. Despite being formally retired from academia, he is frequently invited to speak at conferences or major universities around the world. He speaks English with a strong foreign accent and comes across as a bit grumpy and old-fashioned: for example, he often distributes handwritten notes to his audience instead of using a computer and PowerPoint for his presentations. He also presents his ideas very forcefully and quickly gets defensive when people ask him questions. In his seminars and articles, Zahavi never fails to mention that when he first presented the HP it was unanimously rejected. According to him, the prominent British evolutionary biologist John Maynard Smith agreed to publish his 1975 article in the Journal of Theoretical Biology only to write and publish, less than one year later, a paper of his own to prove that the HP was all wrong. Many other researchers published articles and commentaries that criticized and rejected the HP. According to Zahavi, the main reason for skepticism was that he had initially formulated and expressed the HP in qualitative terms, intuitively, without backing it up with appropriate mathematical models that would show how genetically determined morphological and behavioral traits could evolve and be maintained in populations through the HP. Some evolutionary biologists liked the idea of the HP, but didn’t think it actually worked in the real world. Then, in 1990, a well-regarded evolutionary biologist and mathematician at Oxford University, Alan Grafen, showed mathematically that the Handicap Principle was viable and that this mechanism was consistent with the dynamics of Darwinian evolution. Since then, according to Zahavi, the HP has become widely accepted.10

  Figure 7.1. Dr. Amotz Zahavi. Photo from Wikipedia.

  In reality, the
HP is still controversial and being debated; even the supporting articles written by Alan Grafen have been criticized. Many evolutionary biologists believe that some aspects of the HP are helpful in understanding how communication works and why signals are the way they are. But many are also skeptical about the general validity and applicability of this theory to a wide range of biological phenomena and do not believe, as Zahavi does, that the HP should replace other well-established theories in evolutionary biology, such as reciprocal altruism or kin selection theory.

  As often happens in science, when researchers develop a new theory or a new research approach and think that it can effectively explain some previously unexplained phenomena, they get excited about it and try to apply it to everything else. They announce that the new paradigm will replace old ones and eventually take over entire fields of research or disciplines. This has happened with other paradigms in the behavioral sciences, such as behaviorism and sociobiology. Psychologist B. F. Skinner (1904–1990) was a major supporter of behaviorism—the paradigm that emphasizes the role of learning in behavioral phenomena—and came to believe that the principles of conditioning should be applied to all aspects of human life, from raising children to government. When he tried to argue, in a book called Verbal Behavior (1957), that human languages are learned just like any other aspect of behavior—thus aggressively trespassing into the field of linguistics—this argument prompted a strong negative reaction by linguist Noam Chomsky, who wrote a devastating critique of Skinner’s book.11 Other critiques of behaviorism shortly followed and eventually resulted in the demise of behaviorism as the dominant paradigm in psychology. Similarly, when biologist E. O. Wilson became excited about the power of evolutionary explanations of behavior and announced in his book Sociobiology: The New Synthesis (1975) that sociobiology was going to take over all the other behavioral disciplines, he did more harm than good to the field: sociobiology was criticized on multiple fronts and eventually evolutionary behavioral scientists stopped using this term so that they could work in peace.12 In academia there is a lot of territoriality, and threats of intellectual takeovers by new theories or disciplines inevitably elicit strong defensive reactions; some react with an outright rejection and dismissal of the new paradigm, while others are prompted to an extensive scrutiny of the new paradigm, which usually brings to light some of its weaknesses and limitations.