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

by Dario Maestripieri

  Like many of their illustrious predecessors, in their book The Handicap Principle: A Missing Piece of Darwin’s Puzzle, Amotz Zahavi and his wife Avishag pushed their theory in all kinds of directions and made many claims about the wide range of phenomena this theory could explain. As a result, the book was met with some skepticism and did not become a best seller. Ultimately, however, the usefulness of a scientific theory is judged by the amount of new research and new knowledge that it generates, regardless of whether or not it lives up to its claims or the extent to which its principles are accepted or rejected. In this regard, the HP has generated a great deal of new research and knowledge and therefore must be considered a very influential and successful theory. Amotz Zahavi’s perseverance in presenting and defending the HP, however, incurred the cost of considerable personal and professional strain. In a 2003 article, he made some bitter statements as he noted that living and working in Israel had protected him from the attacks and rejections by his peers, who were mainly based in the United Kingdom and the United States. He wrote: “If I had been dependent on my colleagues for the advancement of my scientific career or my social status, I would not have been able to continue developing the Handicap Principle over the many years in which it was unanimously rejected. Luckily I was living in a corner of the world and . . . at home, my social status and my scientific career were well secured.”13

  Zahavi’s ideas about the testing of social bonds represent one of the relatively minor applications of the Handicap Principle. Essentially, while the HP maintains that individuals have to take on handicaps to prove the reliability of their signals, the bond-testing hypothesis suggests that individuals must impose handicaps on others in order to extract reliable information on their attitudes toward themselves. Unlike other aspects of the HP, the bond-testing hypothesis has not been scrutinized and tested with game-theoretical models that verify whether this mechanism is compatible with and can be supported by known evolutionary processes. Researchers have not systematically gathered data to provide conclusive evidence that animals test their bonds with handicap-related mechanisms. Over the years, however, researchers have accumulated a growing number of observations of seemingly paradoxical behaviors in which animals and humans engage in the context of social bonding, and these behaviors appear to be consistent with Zahavi’s view.

  Eyeball-Poking, Sex, and Other Bizarre Tests of Social Bonds

  Aside from his theoretical work, Amotz Zahavi has observed and studied for many years the behavior of the Arabian babbler, a bird species that lives in Israel. Arabian babblers live in groups of between two and twenty individuals and cooperate in breeding and defending their common territory against neighboring groups. When Zahavi first presented his ideas about bond-testing through the Handicap Principle, he used examples from the species he was most familiar with, the babblers.14 He described how a male sometimes behaves aggressively toward females during courtship; females who are not interested in the male leave his territory and never return, whereas those who have a genuine interest persevere despite the repeated attacks. In Zahavi’s view, this aggression is a handicap that male babblers impose on females to test their suitableness as mates. Zahavi also argued that babblers use allopreening to test the strength of their bonds. One bird preens another, typically a close social companion, pecking at the feathers on his face or body while the recipient remains motionless and facilitates the interaction.

  In reality, these are not great examples of bond-testing. Male aggression toward females in the context of mating and allopreening in birds are better accounted for by other explanations. Males in many animal species, including humans, use aggression toward females as a means of social or sexual coercion. Allopreening in birds is similar to allogrooming in primates, and in both cases these behaviors are effectively accounted for by hygienic and social functions. Examples of animal behaviors do exist for which functions other than bond-testing cannot be easily imagined, but descriptions of these behaviors were not yet available at the time Zahavi published his ideas.

  For a male baboon, fondling another male’s testicles certainly qualifies as an imposition. However, he doesn’t need to place his future reproductive career in a partner’s hand in order to test the strength of their social bond. Wasting time and being stressed are less dangerous but nevertheless costly activities. Annoyance can involve both, so tolerance of annoyance is a good indicator of how much one values a social relationship.

  Capuchin monkeys are small South American primates that live in large groups comprising numerous adult males and females. As with the macaques, baboons, and chimpanzees, capuchin monkeys live in highly competitive societies in which individuals compete for social status through the formation of agonistic alliances. Susan Perry, a primatologist at UCLA who has observed capuchin monkeys in Costa Rica for many years, has reported that these primates periodically test the patience of their favorite social partners—with whom they form aggressive alliances—by subjecting them to all kinds of physically intrusive and annoying behaviors.15 For example, a young capuchin monkey may walk up to his favorite social partner, stick a finger up his nose, and wait for a reaction. If their relationship is good, nothing will happen, but if the partner has lost some of the initial enthusiasm about the partnership, the annoying monkey will get smacked. Perry noticed that two capuchin monkeys who have a strong social bond sometimes simultaneously insert their fingers up each other’s nose and “sit in this pose for up to several minutes with trance-like expressions on their faces, sometimes swaying.” Capuchin monkeys also torture their favorite coalition partners by pulling hairs from their face, biting their ears, or sucking their fingers or toes. In a paper published in 2003 in the journal Current Anthropology, Perry and her colleagues argued that the function of these interactions is to test the strength of social bonds—a positive response from the recipient, or even the toleration of such behaviors, would be indicative of a good relationship and the willingness to further invest in the bond. When these impositions are tolerated, the two partners groom each other for long periods and continue to form alliances against other monkeys.

  At a conference in London in June 2010, Perry showed the audience a video of another bizarre, highly risky, and quite painful bond-testing ritual in capuchin monkeys: two individuals poking each other’s eyeballs. I didn’t attend the conference or see the video, but the journalist Michael Balter wrote the following description:

  One monkey will insert his or her long, sharp, dirty fingernail deep into the eye socket of another monkey, between the eyelid and the eyeball, up to the first knuckle. In videos Perry played for the meeting, the monkeys on the receiving end of the fingernail, typically social allies, could be seen to grimace and bat their eyelids furiously (as did many members of the audience) but did not attempt to remove the finger or otherwise object to the treatment. Indeed, during these eye-poking sessions, which last up to an hour, monkeys insisted on the finger being reinserted if it popped out of the eye socket.16

  If Zahavi’s bond-testing hypothesis does not explain this bizarre behavior, I don’t know what other theory could.

  Susan Perry’s husband, Joe Manson, who is also at UCLA and studies capuchin monkeys with her in Costa Rica, noticed that adult females often touch and briefly hold the infants of females with whom they groom and form aggressive coalitions. Monkey mothers don’t like to have their infants handled this way—there is always a chance that the infant might be harmed—and Manson posited that a mother’s tolerance of this behavior indicates that she values the bond with the female perpetrator and is willing to provide coalitionary support to her. He suggested that the logic of bond-testing could apply to infants as well: when they climb on the back of a female who is not their mother, they are testing this female’s willingness to take care of them, should the need ever arise.17 As we’ll see later, Zahavi argues that human children do this too.

  Figure 7.2. Eyeball-poking ritual between two white-faced capuchin monkeys. Photo courtesy of Dr. Susan Perr
y.

  Bond-testing through risky or annoying intimate interactions is prominent in other animal societies as well. What these societies have in common is individuals forming long-term bonds with others, including the formation of coalitions. Spotted hyenas live in complex societies, called clans, that contain up to eighty individuals who together defend a common territory. Like baboon and capuchin monkey groups, hyena clans are structured by linear dominance hierarchies and contain one to several matrilines of adult females and their offspring, as well as multiple adult immigrant males. The spotted hyena is one of the few species of mammals in which females are dominant over males. They are larger than males, are very aggressive, and have an enlarged clitoris that looks like a penis. In spotted hyena societies, females wear the pants, so to speak. Females acquire and maintain their power through the formation of coalitions with other females.

  In hyena clans, the commitment problem surfaces in the social bonds that sustain cooperation and coalition formation between two females. Hyena females have been observed frequently testing the strength of their partner’s commitment using intimate greeting ceremonies. During these rituals, which last on average twenty seconds but can go on for as long as two or three minutes, two female hyenas stand parallel to one another with their erect penile clitorises, then mutually investigate and sniff each other’s genitalia. When these greetings go wrong, they can result in severe genital wounding. As with the baboons, these are risky interactions in which individuals expose a vulnerable body part to others. A team of spotted hyena researchers at Michigan State University, including Jennifer Smith, Kay Holekamp, and their colleagues, showed that females selectively engage in greetings with their preferred social companions and that these greetings are conducive to the formation of aggressive coalitions against other hyenas of the same clan, joint participation in wars between clans, and cooperative mobbing of lions.18

  One interesting aspect of greetings in spotted hyenas, capuchin monkeys, baboons, and other animals is that they occur at times when bond-testing is most needed, but also when the probability that they might go wrong is reduced. In the spotted hyenas, females spend hours, or even days, apart from their coalition partners while foraging on their own. The greetings typically occur when the partners are reunited in the clan and allow them to test and update their social relationships. African wild dogs hunt in groups, and efficient cooperation is essential for a successful hunt. Research by Scott Creel and his collaborators has shown that greetings between wild dogs typically occur right before the group is about to go hunting.19 If greetings occurred during competitive activities such as feeding or mating, someone might get hurt. So the most likely function of greetings is not to reduce tension at particular times—social animals reduce tension in other ways—but to test the relationship. Observations of greetings in domestic dogs made by Barbara Smuts and her collaborators have shown that dogs greet other dogs most often when there are no immediate resources at stake.20 Thus, greetings appear to offer a mechanism by which animals assess the cooperative tendencies of potential allies in contexts in which the risk of injury is reduced.

  Domestic dogs are totally dependent on their owners, and it’s important for them to test their bonds to know whether they can sleep safe and sound or whether they should worry about being dumped on the street. According to Zahavi, when your dog jumps in your lap and licks your face or gets in the way of what you are doing, he or she is imposing on you to find out how much you still love him or her and are committed to the relationship. The need to gather information is especially important after the owner has been away for a while or is getting ready to leave; these are crucial moments for finding out where the relationship stands. Of course, you might think that when your dog licks your face, he or she is just showing you affection, but one has to wonder why affection is displayed in that particular way.

  Zahavi argues that expressions of love and affection often contain stress-producing, even aggressive elements because the recipient’s acceptance and tolerance of them provides reliable evidence of his or her current willingness to continue to invest in the relationship. In this view, many of the affectionate behaviors shown by children toward their parents, such as jumping on their laps or on their backs, derive their communicative value from being inherently stress-producing.21

  Seen in this light, all of our love signals are impositions of one sort or another: kisses, hugs, and petting intrude on personal space and impair freedom of movement. “Lovers who hold each other’s hand for hours at a time are each giving up the use of a hand for that time, a pretty heavy imposition,” Zahavi says. Lovers who exchange long and passionate kisses stick their tongues in each other’s mouth; that’s quite intrusive and even carries the risk of transmitting disease. Only people who are highly committed to a romantic relationship accept this type of imposition from their partner. According to Zahavi, bond-testing through costly or stressful love signals is frequent especially when the relationship is new and not yet well established, because this is the time when information is most needed. When partners in a long-term relationship stop exchanging French kisses, it may be that they are not as physically attracted to each other as they were at the beginning, but it also could be that their relationship is strong and bond-testing is no longer necessary.

  You will not be surprised to hear, at this point, that Zahavi thinks that sex is the ultimate mechanism for bond-testing. The intrusiveness of many forms of sexual behavior, according to him, makes sex an ideal handicap signal for conveying and receiving detailed information about each lover’s commitment to the relationship. Here I respectfully disagree. Although it is certainly true (if unfortunate) that some people find the intimacy of sexual acts a little uncomfortable, the vast majority of people find the intrusiveness of sex quite pleasant and rewarding. And I doubt that many people would regard holding hands as a heavy imposition. The importance of frequently assessing a partner’s commitment in a romantic relationship, however, cannot be overestimated. This is what an expert on the subject, evolutionary psychologist David Buss, argues in his book The Dangerous Passion: Why Jealousy Is as Necessary as Love and Sex:

  Commitments can change from day to day as a function of an individual’s financial situation, or reputation, or age, health, stress, or status. A woman who overestimates her lover’s commitment risks abandonment, damage to her reputation, and the hard work of raising a child alone. Overestimating commitment also leads to opportunity costs: the time spent with an undercommitted partner reduces the chance to attract a better mate. Underestimating the true level of a partner’s commitment can also be costly, leading to a self-fulfilling prophecy. Miscalculating, for example, could cause you to reduce your own commitment, impelling your partner to do the same, thereby producing a downward spiral of mutual retreat and resentment. The bitter result could dissolve the relationship as both partners search their social world for deeper, more meaningful engagement.22

  Zahavi’s contention that love expressions, including sex, are wasteful, risky, stressful, or even painful impositions—all the properties of handicaps—seems a little pessimistic, but to wonder why romantic partners express their love by sticking their tongues in each other’s mouths instead of, say, playing chess together is to ask a legitimate question that, if nothing else, provides food for thought. Zahavi has also made the less controversial suggestion that his bond-testing hypothesis explains why old friends sometimes tease and insult or slap and hit each other.23 Verbal and physical offenses are clearly impositions that only an old friend who is quite committed would tolerate. In the film Gran Torino, the main character, played by Clint Eastwood (who also directs the film), is a grumpy old Korean War veteran named Walt who is trying to teach his young apprentice, a Hmong teenager named Thao, how to navigate social life. Walt is friends with a barber in his neighborhood, and the two of them exchange banter and racial insults every time they see each other. One day Walt brings Thao into the barber’s shop, and after greeting his friend with racial slurs a
s usual, he turns to Thao and says to him: “You see, kid, that’s how guys talk to one another. Now go out, come back in, and talk to him like a man, like a real man.” Thao reluctantly does as he is told: he walks back into the shop and says to the barber, “What’s up, you old Italian prick?” The barber gets mad at Thao and threatens to blow his head off with a rifle. The scene nicely illustrates the principle behind Zahavi’s bond-testing hypothesis: one is willing to tolerate an imposition from a good friend but not from a stranger; thus, imposing on another individual can provide reliable information about the quality of your relationship.