Carter was also jet-lagged, having flown home the day before from Morocco, but she nonetheless had agreed to a conversation in her new town house just outside Chapel Hill, North Carolina, where she recently moved her work after spending most of her career as a neurobiologist at the University of Chicago. She takes a spot on a comfortable couch and is quickly joined by her Chin, a Japanese spaniel lapdog. And then she decides to begin where her work began in the 1970s: with prairie voles, an innocuous and silent mouselike species that navigates the tangled plant world of North American grassland ecosystems, mostly unseen by all except owls and biologists.
She began working in association with the field biologists who were asking the questions common in that discipline in the 1970s, questions that mostly had to do with survival and crashing population—and, when evolutionary ideas came into the picture, with the physical makeup of the beast in question, because then the emphasis was on finding those physical attributes that conferred fitness. At that time, prairie voles were undergoing boom-and-bust cycles—population explosions followed by crashes; it’s the sort of phenomenon that alarmed biologists then but is now better understood as the normal course of events, especially among ground-level rodents. But the researchers quickly came to understand that there was something truly odd about this obscure little species of rodent. They were social. There was a vibrant vole society, and holding it together was monogamy (or at least that’s how it looked from a hawk’s-eye view), strong pair bonds between a single male and a single female, which is an uncommon practice among mammals.
What is most curious about this is that meadow voles—a closely related but separate species, the same genus in the same habitat—are not monogamous. All but a trained biologist—even owls—would be hard-pressed to spot the difference between a prairie vole and a meadow vole, yet prairie voles go in for lifelong bonding to a single mate and meadow voles do not. In the ’70s monogamy was thought to be a complex, evolved behavior like bipedalism or omnivory, and so followed an evolutionary line and logic in a predictable progression. But here it was, a distinctive behavior dropped into a single species without warning, like a plug-in option in a new model year of a car.
Back then, though, evolutionary biologists had a ready explanation for monogamy, rare as it was in mammals—an explanation based in sexual selection. That is, a male bonds to a given female and invests his energy in raising the young because they are his genetic issue. This in turn is rooted in the idea of what is famously labeled the “selfish gene,” meaning that evolution selects for genes that perpetuate themselves and so selects for individuals that ensure perpetuation of their own genes over those of others. This, for instance, is the common explanation for the widespread practice of infanticide in the animal world, including among human animals: males, on encountering a new female, often kill her young so that they might replace them with their own genetic issue. In most cultures, including ours, death rates among children with stepfathers are about equal to those among other mammals.
Even in her early work, though, Carter was skeptical of this explanation for monogamy in prairie voles. “I had been exposed to enough sociobiology and evolutionary biology to assume that reproduction was the core of evolutionary theory. I don’t think it is true. I think it is actually social interactions that are driving many aspects of behavior,” she told us.
She was right, but it was not until the 1980s and the availability of certain tools for analyzing DNA that the fuller story emerged. Monogamous in outward appearances these prairie voles might be, but the undeniable evidence of the genes of vole pups demonstrated that these loyal males laboring their lives away raising pups were in fact cuckolds. About half of the pups were not their genetic issue. What’s more, this rough ratio held up across the animal kingdom, especially among birds, for which monogamy is far more common. Depending on whom you ask and when, you will likely as not be told that humans are monogamous, but if you ask DNA about this, the story is much the same as for other animals. Sexually monogamous? Well, no. Voles and all the rest of the animals prefer marriage of convenience, which does not mean that the concept of monogamy is irrelevant, but it does need refining. It does not describe a sexual behavior, an adaptation based in reproduction. Rather, it describes a social adaptation that is indeed useful in ensuring a next generation, even a selfish gene generation. Half of the kids might not be the kin of papa vole, but half of them are, and stable social arrangements make everybody better off.
Yet this realization meant that the inquiry had wandered into what was then shaky ground for biologists, who were used to considering issues like prey base, carrying capacity, length of stride, and length of fang. Monogamy was not a physical attribute; it was a behavior. But the evidence was saying that the behavior was innate, not learned. But more to the point, vole society started to uncannily resemble that of humans, and no one really had any idea where that came from.
“They have a social system that looks like humans’: long-lasting pair bonds, two parents taking care of young, incest avoidance, extended families—just about everything that is cardinal to human society,” Carter said.
But not all of them, and not all of their lives. There are a couple of modes of prairie vole living, and all of this talk of sex completely ignores something important: those voles that ignore sex. This is a common thread in all social animals, even termites and ants. We have long wondered why so many members of, say, a bee colony are simply not players in reproduction, that task being relegated to the few fertile: a queen and the several drones who are her mates. Most bees go through life oblivious to mating, and it is not that different with voles. Most of these rodents spend life in what Carter labeled a “prepubertal” stage. But biologists soon discovered what flipped that switch: a simple matter of a timely meeting with an appropriate mate. Each half of the budding couple discovers the other by chance while they are still in that prepubertal state, but the encounter itself triggers a response in each that looks very much like going through puberty. The male especially is completely transformed in a matter of hours from a clueless, sexless naïf to a rather fiercely attached partner, and the partnership lasts for life. At the root of this transformation, Carter figured out, was oxytocin and, especially in the male, vasopressin. These are two closely related biochemicals, technically neuropeptides (brain chemicals). This discovery alone ratchets up the relevance of the finding to the human condition: oxytocin is the most common gene-generated molecule in the human brain. In voles, it is the transformative switch.
And not just in prairie voles, it turns out, and this is in many ways the finding that nailed the centrality of this single molecule in the foundational behavior of a whole series of widely unrelated species. That initial work with prairie voles has spawned what Carter characterizes today as a “tsunami” of research. Literally hundreds of labs worldwide are working on this single molecule, but one of the early eureka experiments involved giving oxytocin to species such as rats. Males of this species are not given to hanging around rearing young and helping out with the housework. These males are by nature more inclined to be, well, rats—but oxytocin-dosed rats adopted monogamous habits, including attentive pup rearing. Even in the close relative of prairie voles, the meadow voles, tweaking their brains to enhance their ability to feel the effects of oxytocin caused exactly the same behavioral shift.
The initial research about oxytocin predated the work on voles. As early as the 1950s, the neuropeptide had been identified and cited for its role in birth, lactation, and even sexual attraction. Further work in sheep and rats in the 1970s showed oxytocin’s role in bonding between mothers and young rats and sheep. Yet demonstrating oxytocin’s ability to organize the social system of prairie voles has tipped off scientists to roles for this single molecule far beyond the fundamentals of intercourse and reproduction.
It is the social molecule, and interest in it has built to something of a fever pitch with the realization that, although the molecule is manufactured deep in the brain and h
as its most profound effects there, it need not be injected directly into the brain, as was painstakingly done in the early research. It works its magic administered as a simple nasal spray, which is by far the most direct route to the brain, as cocaine users know. Some substances that we inhale quickly enter the brain, as we talked about with the aromas of nature in the last chapter.
As a practical matter, this has made the experiment with human subjects easier and a lot less invasive, ramping up this line of inquiry. Notably, experiments using standard tests for altruism, exactly like those we saw with meditation and exposure to nature, have delivered clear demonstrations that oxytocin enhances empathy and altruism. Oxytocin made subjects more likely to part with their money to offset what they saw as unfairness to another person. Oxytocin also enhances what psychologists call social cognition—that is, social skills. For instance, we can easily see how—and research has demonstrated this—our social bonds are dependent on our brain’s ability to recognize faces, and oxytocin enhances that ability. It also enhances the ability to identify emotional states as they are displayed on faces, meaning the ability to read emotions in others. A whole series of experiments has shown the molecule’s ability to enhance trust in others, and this idea expands how we might think about the importance of social relationships.
Research has also shown that oxytocin plays a key role in business transactions, especially in establishing trust. This is not as squishy as it might sound. Economists will tell you that the workings of the marketplace depend on a foundation of trust, that the glue of our economic lives rests on our ability to trust one another well enough to do deals. Follow this idea backward now through evolutionary time, and you can begin to see where this winds through the human condition, and how this group cohesion is part of our evolutionary success, our ability to adapt and prosper. Trust enables economy, a rule best demonstrated in negative examples, in places where anarchy and chaos have undermined all trust. Those places have little hope of economic development.
There are a couple of interesting asides in this same line of research. People engaged in business transactions produce a spurt of oxytocin. If one person gives another person ten dollars, the recipient’s oxytocin levels spike a bit. But here’s the kicker: if a computer gives that same person ten dollars, his levels of oxytocin do not increase. And there’s a bit of intraspecific research that is our personal favorite: if you engage your dog, your oxytocin level increases, as you might expect—but your dog’s oxytocin level increases even more.
Take these realizations together, and it’s easy to see how some of them might provoke a scientific feeding frenzy. You can get a hint of this in the appearance of a recent popular book about oxytocin that’s gushing with promise and titled The Moral Molecule. This chemical begins to look like a magic bullet, especially to people with autism. Remember, autism is characterized by that very lack of social ability that seems at the center of oxytocin’s field of expertise. Things like enhancing the ability to recognize facial cues and other such social skills can seem like exactly what the doctor might order, and, in fact, some work has been done with autistic people that encourages this conclusion. So here appears an inviting target right up the center of the medical model’s line of thinking: an easily synthesized molecule that can be administered in a simple nasal spray, is already the most common molecule in the human brain, and deals straight on with one of modern medicine’s most intractable maladies—and at the same time spins off into trust, empathy, love, and understanding. What’s not to love? What’s not to love for Big Pharma?
Science magazine caught this drift in an article in January 2013 that began as follows:
Few substances produced by the human body have inspired as much hoopla as oxytocin. Recent newspaper articles have credited this hormone with promoting the kind of teamwork that wins World Cup soccer championships and suggested that supplements of the peptide could have prevented the dalliances and subsequent downfall of a certain high ranking U.S. intelligence official. Although the breathless media coverage often goes too far, it reflects a genuine and infectious excitement among many scientists about the hormone’s role in social behavior.
Well, maybe, but haven’t we been down this road before, seen the allure of magic-bullet, single-pathway solutions?
Or as Carter put it: “The public wants a fast answer. If we know it works, why don’t we make a drug out of it [oxytocin]?” She added that such a solution “seems a bit arrogant and stupid.”
To begin with, we’ve known from the very beginning of the work on voles that if you focus on the yin of oxytocin and ignore the yang of vasopressin, you are going to miss some key elements. And, in fact, yin-yang probably overstates the separation, because both neuropeptides are very closely related in function, chemical structure, and evolutionary history. Both are important to both genders, but vasopressin has a decidedly male skew.
This is probably more than an interesting aside because everything in the human body is connected, but vasopressin research also appears in a very different arena, one that explores its function as a regulator for water. In its finer points, however, this regulation by vasopressin (which is in its chemical structure almost identical to oxytocin) turns out to be far more interesting and, in fact, seminal to some of our earlier discussions about exercise. Vasopressin is what gave us the ability to practice the form of persistence hunting that David Carrier (the mountain runner–researcher at the University of Utah) talked about and what helped him begin to understand why humans were born to run. We developed this skill in an arid landscape, after all. Modern bushmen still do persistence hunting in the desert, and observers have noticed that they do it without drinking water. Thomas, in fact, noted that groups of men who hunt and women who go on daylong forays of gathering food take nothing more than an ostrich eggshell full of water to last the whole day under a desert sun. That is to say, these bushmen could run full days in scorching heat on an amount of water that some people advise modern runners to drink every half hour.
The South African researcher Tim Noakes has done an extensive study of this matter and has shown pretty clearly that the more excessive modern advice on runners and water is, in fact, just that: excessive. The data show that the advice to drink lots of water (actually to “hydrate,” and that’s part of the problem—that we no longer drink water; we “hydrate”) is simply wrong. Noakes’s analysis showed that runners who were the most dehydrated after marathon-length races actually tended to win. More to the point, no one suffered medical problems from dehydration, while those who drank the recommended amount of water or sports drinks often suffered severe consequences from too much water. Some even died.
The deal is, exercise, especially running in hot conditions, triggers a cascade of vasopressin, which causes the runner’s body to conserve water. That’s the very trick that allowed the bushmen to succeed in the desert, and the deaths in modern-day marathons are the result of our thinking that we need a solution like “hydration” to overrule evolution’s design. One more example.
But the more telling bit of information in this aside is evidence that both vasopressin, as we have shown, and oxytocin, the “social molecule” we are trying to bottle in nasal sprayers, are triggered by exercise. Chalk up one more brain benefit from exercise. And by now, it should be no surprise that running, movement, social bonding, and emotional well-being have a common chemical pathway. Chemically, these seemingly disparate topics hang together, and we ought to pay attention to that as a big signpost of evolution’s design.
But back to the social side of this chemistry. Many of the effects that produce monogamy in voles are triggered not just by oxytocin but by the right balance of oxytocin and vasopressin. In all of this, there is not a straightforward, dose-dependent response to oxytocin, no rule that says more oxytocin yields more warm and fuzzy behavior. Rather, these adaptive social traits emerge from a complex dance between the two neuropeptides—at least these two—and then play into a cascade of hormones. And all is gen
der-dependent.
But a second element of this discussion looms even larger. Oxytocin and vasopressin are molecules that carry a signal of sorts, and there need to be receptors in the brain specific to each molecule. The number and efficacy of these receptors have much to do with how the brain reads and accomplishes the effects called for in the cascade of these molecules and all the other neuropeptides that the body uses to regulate the mind. Indeed, the research has targeted these very receptors from the beginning. For instance, researchers, as we said, were able to make the normally inattentive and philandering male meadow voles behave like the monogamous and responsible prairie voles. But they did so not by amping up oxytocin levels but by genetically engineering vole brains for better receptors. Oxytocin is a universal chemical in vertebrate life, but the differences among the various species’ behaviors are due in part to variations in receptors, not levels of oxytocin. This also explains why the trait of monogamy is not a neat, linear progression through evolutionary family trees, but rather pops up here and there. Genes that build the receptors kick in and out, like toggle switches.
Researchers also believe that the variability in receptors helps explain differences within species, why one individual is more touchy-feely than another. This is not the sole explanation. As we have seen, exercise or encountering the right mate triggers spikes in oxytocin, but genes play a role as well. Genes control, at least in part, the number of receptors, and that very idea is why Carter bristles at the current simplistic line of research that says all we need to do is spritz a bit of oxytocin up one’s nose to provoke a lifetime of sweetness and light. Her caution is based on some hard research and some personal experience.
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