Recently on the 7-12-11 Colbert Report, Stephen Colbert interviewed advice columnist Dan Savage about monogamy and fidelity. Dan passionately advocated that sexuality in relationships can and should be negotiated, with everything on the table including monogamy. He referred with some pride to a three-way sexual encounter he’d had with his lover and another man as an example of how extramarital sex could be a good thing in relationships. I found their exchange entertaining and refreshing. I love seeing intelligent people have open discussions about sex, relationships, and intimacy in general, and I think our culture benefits from such talk. I understand that the complexities of development and sexual bonding can’t be adequately addressed in an eight-minute comedy dialogue, so I want to add a few points to their conversation. People relate differently depending on lots of variables including sexual orientation, age, maturity, and emotional stability. For instance, research by John Gottman found that gay couples (like Dan and his lover) typically have less hostility and more humor dealing with conflict, and are better able than other groups to talk openly about sex and fidelity. Further, I’ve found that younger couples without children are more likely to sexually experiment both secretly (affairs, infidelity), and openly (three-ways, non-exclusive relationships). This might explain why divorce is most common in childless twenty-something first marriages. Dan Savage’s implication that honest negotiation can make for happy non-exclusivity in relationships misses a few neurobiological and evolutionary points. How you feel about non-monogamous sex has everything to do with how your nervous system holds a sexual relationship. We’re programmed for lust for any attractive other, romantic infatuation with a special other, and intimate bonding with someone we have become sufficiently close with over time. These are three separate systems that are intertwined, but also have their own emotional patterns and demands. Lust tends to be more easily promiscuous and non-exclusive. People generally don’t get particularly sexually possessive about someone they are simply having sex with, but with whom they haven’t entered a state of romantic infatuation or intimate bonding. This is why a prostitute’s customers rarely feel jealous of other customers, why a college student waking next to someone he or she picked up the night before for a casual hook up is unlikely to feel jealous of whoever else has shared this bed, and why 40% of single women from 19 to 39 have a guy they call occasionally for sex with no hint of monogamy. Romantic infatuation occurs when your nervous system decides that this person is a very special lover—someone we specifically hunger for. Now a guy who previously didn’t care much if his lover dated other guys gets jealous if she just smiles at another man, never mind has sex with him. A woman who’s previously enjoyed casual hookups without complications finds herself thinking about her lover all the time and can’t get enough contact, sex, and intimacy with him. Most people in states of romantic infatuation aren’t much interested in sex with others, and suffer badly if their lover strays. When you are in the intimate bonding stage of a relationship—which often follows an initial one-to-four year romantic infatuation joyride—sex and romance become less urgent and easy. The excitement/sexy neurotransmitters dopamine and testosterone are down, and the bonding/attachment neurotransmitters oxytocin and vasopressin are up, and people feel more securely connected while less obsessively “in love.” Even though you feel less sexually urgent, intimate bonding is important—as in life-partner important. If you find out your partner has cheated, your nervous system freaks out into jealousy, depression, obsession, and outrage. On the other hand, since most of us crave the heat of desire and infatuation, even in satisfying intimate bonding we can find ourselves longing for the sweet rushes of lust and romance (these are the forces that cause us to seek loopholes in our monogamy commitments). We can amplify lust and romance in intimate bonding, but it usually requires two people putting in some effort. For example, since change, risk, and excitement raise dopamine (and correspondingly testosterone) levels, people often get sexual boosts from novel experiences they share with their intimate partner. These can range from roller coasters, to hotel rooms, to vacations, to having your wife’s old college roommate join you in bed. ` The problem with bringing other sexual partners into an intimate relationship is that it messes with our evolutionary programming in potentially disastrous ways. Once you start having sex with someone, you risk moving into romantic infatuation where they specifically take on romantic luminance. Remember, we can lust for one person, be “in love” with another, and be intimately bonded with a third—they are three distinct systems. It might be OK with you and your wife to have a three-way with her friend, but your wife will go crazy if you and her friend fall in love. Similiarly, if your wife has brief fling at a conference, it might be a trivial sexual adventure to her, but it will drive you crazy that she cheated on you. Dan Savage reprises the familiar refrain of, “If we just talk about it like rational adults, almost anything is possible.” This reminds me of a horrible night I spent in the summer of 1975 when Becky and I were trying to have a non-exclusive relationship (after heroic efforts to the contrary, we eventually decided we were monogamous). My friend Noel had approached me to see if I would mind if he asked Becky out, and I foolishly answered, “Why not? We’re all sexually liberated adults. We’re not bound by the conventions of the past. It’s up to her.” I remember feeling particularly free saying this to Noel, not knowing what was to come. Like a slow motion train wreck, events gradually unfolded over the next week. Noel asked Becky out. Becky talked with me about it and I gave her the same new-age non-exclusive rap. The night arrived and they went out. And here I was, driving my Rambler Ambassador alone through the summer night, smelling orange blossoms on the sweet night air, and trying unsuccessfully to not think of them up at Noel’s house at the top of San Marcos Pass, making love on the bed he had suspended beneath a skylight that opened the room to the moon and stars. As I kept trying the manage the shocking waves of grief, rage, and sexual frustration that washed over me, I told myself, “Keith, remember this. Some things you can’t negotiate.” It wasn’t until decades later that anthropology and neurobiology revealed the genetic roots of my suffering. Suffice to say, Becky and I had a long talk and she stopped dating Noel. Noel, in just that one night, fell for Becky (I can’t blame him, she’s great), and essentially stalked her the next several months. He eventually had enough presence to stay away and get over it. I—stubborn and arrogant young man that I was—needed to get my emotional ass kicked a few more times before I realized that, once the romantic infatuation/intimate bonding circuits are activated, multiple partners aren’t going to work. Becky and I finally got it and have been happily monogamous ever since. Sex and romance are drives that can light up irresistible evolutionary forces. The statistics tell the story. A million women and four hundred thousand men report being stalked every year in America, mostly involving erotic attachments (and that’s just the tip of the iceberg since people often don’t report stalking). Untold depression and suicide comes from romantic betrayal and relationship breakups. Over 25% of murders in this country involve lovers, spouses, and love triangles—the darkest reflection of the power of sexual bonding. We can play pretend games and gamble with our biochemistry—sometimes successfully as in the three-way that actually doesn’t leave anybody feeling distressed, ripped off, or deserted—but for the most part when you play with sexual fire, people get burned. You can’t reason your nervous system out of millions of years of evolutionary conditioning. Save such miracles for masturbation fantasies—usually harmless sources of sexual/romantic variety. In the real world, partners can harmonize, adjust, and support each other to keep sex growing and romance alive, but you can’t reverse or ignore biological drives just because it sounds like it might be fun. Someone usually gets hurt.