In ancient Rome, two men taking an oath of allegiance held each other's testicles, and men held their own testicles as a sign of truthfulness while bearing witness in a public forum. The Romans found a word to describe this practice but didn't invent the practice itself. Other primates had already been doing this for millions of years. Two male baboons who cooperate with each other by forming aggressive alliances against other baboons frequently fondle each other's genitalia. This behavior has nothing to do with sex but it's a social ritual that primatologists call a "greeting." The behavior of ancient Romans and male baboons can be explained by the Handicap Principle, an evolutionary theory according to which the most effective way to obtain reliable information about a partner's commitment in a relationship - whether a political alliance, a romantic relationship, or a business partnership - is to impose a cost on the partner and assess the partner's willingness to pay it.
To better understand the testicle ritual and its explanation, it's important to remember that cooperative relationships between unrelated individuals are intrinsically unstable: one business partner may cooperate one moment and cheat in another, and one romantic partner may promise eternal commitment one day and end the relationship the next. Economists call this "the commitment problem." Because of the commitment problem, two partners must frequently assess the strength of their bond, in order to decide whether to continue investing in the joint venture or bail out. The most direct way for romantic partners to assess their mutual commitment is simply to ask each other, "Are you sure you still love me?" or "Are you sure you want to be with me forever?" Couples in love do this all the time 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.
Evolutionary biologist Amotz Zahavi, the father of the Handicap Principle, has suggested 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. In nature, the equivalent of money is fitness: the ability to survive and reproduce. Therefore, the best way for an animal to address the commitment problem in a cooperative relationship is to assess the extent to which a partner is willing to risk his or her survival or future reproduction to maintain that relationship. In other words, testing the strength of the bond involves behaving in ways that are costly, risky or otherwise detrimental to the partner.
When two male baboons, let's call them Bill and Bob, fondle each other's genitalia, they both take a huge risk. By letting Bob fondle his testicles, Bill shows a great deal of trust in Bob's good intentions. Bob could quickly and easily terminate Bill's reproductive career for good by ripping his testicles off. On the other hand, by getting so close to Bill and attempting to touch his testicles, Bob exposes himself to a high risk of aggression. A single bite inflicted with Bill's sharp canines could scar Bob 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. By taking the risk and tolerating the imposition, two male baboons demonstrate how much they value their relationship. A male baboon who wants to measure precisely his partner's commitment to their alliance 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.
Given how risky greetings are, the performance of these rituals requires a great deal of caution. In an article published with my former Ph.D. student Jessica Whitham, we showed that pairs of adult males with poor or unstable relationships either don't exchange greetings at all or their greetings are often aborted. 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. Barbara Smuts, another researcher who has studied greetings between male baboons, noticed 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.
The fondling of genitalia by male baboons is by no means the only ritual with which animals test the strength of their bonds with their favorite social partners. Over the years, researchers have accumulated a growing number of observations of seemingly paradoxical social behaviors that appear to be consistent with Zahavi's bond-testing hypothesis. Capuchin monkeys are small South American primates that live in highly competitive societies in which individuals gain and maintain 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 alliance partners by subjecting them to all kinds of physically intrusive and annoying behaviors. 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. 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, 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 Michael Balter, a reported for Science magazine, 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".
Well, if you think monkeys use bizarre behaviors for bond-testing purposes, according to Zahavi we human beings have come up with far more bizarre, intimate, risky, and annoying ways to make sure our romantic partners are committed to the relationship (to be continued).