As I said, it takes a lot of work to cure people of that physics envy, and to see that interindividual differences in testosterone levels don’t predict subsequent differences in aggressive behavior among individuals. Similarly, fluctuations in testosterone levels within one individual over time do not predict subsequent changes in the levels of aggression in that one individual—get a hiccup in testosterone secretion one afternoon and that’s not when the guy goes postal.
Look at our confusing state: normal levels of testosterone are a prerequisite for normal levels of aggression, yet changing the amount of testosterone in someone’s bloodstream within the normal range doesn’t alter his subsequent levels of aggressive behavior. This is where, like clockwork, the students suddenly start coming to office hours in a panic, asking whether they missed something in their lecture notes.
Yes, it’s going to be on the final, and it’s one of the more subtle points in endocrinology—what is referred to as a hormone having a “permissive effect.” Remove someone’s testes and, as noted, the frequency of aggressive behavior is likely to plummet. Reinstate precastration levels of testosterone by injecting that hormone, and precastration levels of aggression typically return. Fair enough. Now this time, castrate an individual and restore testosterone levels to only 20 percent of normal and . . . amazingly, normal precastration levels of aggression come back. Castrate and now generate twice the testosterone levels from before castration—and the same level of aggressive behavior returns. You need some testosterone around for normal aggressive behavior—zero levels after castration, and down it usually goes; quadruple it (the sort of range generated in weight lifters abusing anabolic steroids), and aggression typically increases. But anywhere from roughly 20 percent of normal to twice normal and it’s all the same; the brain can’t distinguish among this wide range of basically normal values.
We seem to have figured out a couple of things by now. First, knowing the differences in the levels of testosterone in the circulation of a bunch of males will not help you much in figuring out who is going to be aggressive. Second, the subtraction and reinstatement data seem to indicate that, nevertheless, in a broad sort of way, testosterone causes aggressive behavior. But that turns out not to be true either, and the implications of this are lost on most people the first thirty times you tell them about it. Which is why you’d better tell them about it thirty-one times, because it is the most important point of this piece.
Round up some male monkeys. Put them in a group together, and give them plenty of time to sort out where they stand with each other—affiliative friendships, grudges and dislikes. Give them enough time to form a dominance hierarchy, a linear ranking system of numbers 1 through 5. This is the hierarchical sort of system where number 3, for example, can pass his day throwing around his weight with numbers 4 and 5, ripping off their monkey chow, forcing them to relinquish the best spots to sit in, but, at the same time, remembering to deal with numbers 1 and 2 with shit-eating obsequiousness.
Hierarchy in place, it’s time to do your experiment. Take that third-ranking monkey and give him some testosterone. None of this within-the-normal-range stuff. Inject a ton of it into him, way higher than what you normally see in a rhesus monkey; give him enough testosterone to grow antlers and a beard on every neuron in his brain. And, no surprise, when you then check the behavioral data, it turns out that he will probably be participating in more aggressive interactions than before.
So even though small fluctuations in the levels of the hormone don’t seem to matter much, testosterone still causes aggression. But that would be wrong. Check out number 3 more closely. Is he now raining aggressive terror on any and all in the group, frothing in an androgenic glaze of indiscriminate violence? Not at all. He’s still judiciously kowtowing to numbers 1 and 2, but has simply become a total bastard to numbers 4 and 5. This is critical: testosterone isn’t causing aggression, it’s exaggerating the aggression that’s already there.
Another example just to show we’re serious. There’s a part of your brain that probably has lots to do with aggression, a region called the amygdala.9 Sitting right near it is the Grand Central Station of emotion-related activity in your brain, the hypothalamus. The amygdala communicates with the hypothalamus by way of a cable of neuronal connections called the stria terminalis. No more jargon, I promise. The amygdala has its influence on aggression via that pathway, with bursts of electrical excitation called action potentials that ripple down the stria terminalis, putting the hypothalamus in a pissy mood.
Once again, do your hormonal intervention; flood the area with testosterone. You can do that by injecting the hormone into the bloodstream, where it eventually makes its way to this part of the brain. Or you can be elegant and surgically microinject the stuff directly into this brain region. Six of one, half a dozen of the other. The key thing is what doesn’t happen next. Does testosterone now cause there to be action potentials surging down the stria terminalis? Does it turn on that pathway? Not at all. If and only if the amygdala is already sending an aggression-provoking volley of action potentials down the stria terminalis, testosterone increases the rate of such action potentials by shortening the resting time between them. It’s not turning on the pathway, it’s increasing the volume of signaling if it is already turned on. It’s not causing aggression, it’s exaggerating the preexisting pattern of it, exaggerating the response to environmental triggers of aggression.
This transcends issues of testosterone and aggression. In every generation, it is the duty of behavioral biologists to try to teach this critical point, one that seems a maddening cliché once you get it. You take that hoary old dichotomy between nature and nurture, between biological influences and environmental influences, between intrinsic factors and extrinsic ones, and, the vast majority of the time, regardless of which behavior you are thinking about and what underlying biology you are studying, the dichotomy is a sham. No biology. No environment. Just the interaction between the two.
Do you want to know how important environment and experience are in understanding testosterone and aggression? Look back at how the effects of castration were discussed earlier. There were statements like “Remove the source of testosterone in species after species and levels of aggression typically plummet.” Not “Remove the source . . . and aggression always goes to zero.” On the average it declines, but rarely to zero, and not at all in some individuals. And the more social experience an individual had being aggressive prior to castration, the more likely that behavior persists sans cojones. Social conditioning can more than make up for the hormone.
Another example, one from one of the stranger corners of the animal kingdom: If you want your assumptions about the nature of boy beasts and girl beasts challenged, check out the spotted hyena. These animals are fast becoming the darlings of endocrinologists, sociobiologists, gynecologists, and tabloid writers. Why? Because they have a wild sex-reversal system—females are more muscular and more aggressive than males and are socially dominant over them, rare traits in the mammalian world. And get this: females secrete more of certain testosterone-related hormones than the males do, producing the muscles, the aggression (and, as a reason for much of the gawking interest in these animals, wildly masculinized private parts that make it supremely difficult to tell the sex of a hyena). So this appears to be a strong vote for the causative powers of high androgen levels in aggression and social dominance. But that’s not the whole answer. High up in the hills above the University of California at Berkeley is the world’s largest colony of spotted hyenas, massive bone-crunching beasts who fight with each other for the chance to have their ears scratched by Laurence Frank, the zoologist who brought them over as infants from Kenya. Various scientists are studying their sex-reversal system. The female hyenas are bigger and more muscular than the males and have the same weirdo genitals and elevated androgen levels that their female cousins do back in the savannah. Everything is in place except . . . the social system is completely different from that in the wild. D
espite being stoked on androgens, there is a very significant delay in the time it takes for the females to begin socially dominating the males—they’re growing up without the established social system to learn from.
When people first grasp the extent to which biology has something to do with behavior, even subtle, complex, human behavior, there is often an initial evangelical enthusiasm of the convert, a massive placing of faith in the biological components of the story. And this enthusiasm is typically of a fairly reductive type—because of physics envy, because reductionism is so impressive, because it would be so nice if there were a single gene or hormone or neurotransmitter or part of the brain that was it, the cause, the explanation of everything. And the trouble with testosterone is that people tend to think this way in an arena that really matters.
This is no mere academic concern. We are a fine species with some potential. Yet we are racked by sickening amounts of violence. Unless we are hermits, we feel the threat of it, often as a daily shadow. And regardless of where we hide, should our leaders push the button, we will all be lost in a final global violence. But as we try to understand and wrestle with this feature of our sociality, it is critical to remember the limits of the biology. Testosterone is never going to tell us much about the suburban teenager who, in his after-school chess club, has developed a particularly aggressive style with his bishops. And it certainly isn’t going to tell us much about the teenager in some inner-city hellhole who has taken to mugging people. “Testosterone equals aggression” is inadequate for those who would offer a simple solution to the violent male—just decrease levels of those pesky steroids. And “testosterone equals aggression” is certainly inadequate for those who would offer a simple excuse: Boys will be boys and certain things in nature are inevitable. Violence is more complex than a single hormone. This is endocrinology for the bleeding heart liberal—our behavioral biology is usually meaningless outside the context of the social factors and environment in which it occurs.
FURTHER READING
For a good general review of the subject, see E. Monaghan and S. Glickman, “Hormones and Aggressive Behavior,” in J. Becker, M. Breedlove, and D. Crews, eds., Behavioral Endocrinology (Cambridge, Mass.: MIT Press, 1992), 261. This also has an overview of the hyena social system, as Glickman heads the study of the Berkeley hyenas. For technical papers on the acquisition of the female dominance in hyenas, see S. Jenks, M. Weldele, L. Frank, and S. Glickman, “Acquisition of Matrilineal Rank in Captive Spotted Hyenas: Emergence of a Natural Social System in Peer-Reared Animals and Their Offspring,” Animal Behavior 50 (1995): 893; and L. Frank, S. Glickman, and C. Zabel, “Ontogeny of Female Dominance in the Spotted Hyaena: Perspectives from Nature and Captivity,” in P. Jewell and G. Maloiy, eds., “The Biology of Large African Mammals in Their Environment,” Symposium of the Zoological Society of London 61 (1989): 127.
I have emphasized that while testosterone levels in the normal range do not have much to do with aggression, a massive elevation of exposure, as would be seen in anabolic steroid abusers, does usually increase aggression. For a recent study in which even elevating into that range (approximately five times normal level) still had no effect on mood or behavior, see S. Bhasin, T. Storer, N. Berman, and colleagues, “The Effects of Supra-physiologic Doses of Testosterone on Muscle Size and Strength in Normal Men,” New England Journal of Medicine 335 (1996): 1.
The study showing that raising testosterone levels in the middle-ranking monkey exaggerates preexisting patterns of aggression can be found in A. Dixson and J. Herbert, “Testosterone, Aggressive Behavior and Dominance Rank in Captive Adult Male Talapoin Monkeys (Miopithecus talapoin),” Physiology and Behavior 18 (1977): 539. For the demonstration that testosterone shortens the resting period between action potentials in neurons, see K. Kendrick and R. Drewett, “Testosterone Reduces Refractory Period of Stria Terminalis Neurons in the Rat Brain,” Science 204 (1979): 877.
The Graying of the Troop
Bill Martin, Transitions, 1978; courtesy Joseph Chowning Gallery, San Francisco
It was one of those days when all his joints ached. The rains had started, and the humidity inflamed his hips and knees, especially the one he had injured long ago in his youth. He hobbled across the field, off to find something to eat and then, perhaps, to sit with a friend. Foraging for palatable food had grown more difficult as he lost more of his teeth—sometimes he spent half the day trying to appease his hunger. He paused for a moment, a bit disoriented, briefly unsure of his direction. When he was young, he had sprinted and chased and wrestled with his friends in this field.
As he resumed on the path, the two of them emerged from behind a tree, coming toward him. He tensed. They were new to the area, strangers, but not quiet like new ones usually were. Instead they were confident, making trouble for everyone. They worked together. Maybe they were brothers.
He was frightened, breathing faster. He hesitated for an instant to scratch nervously at a sudden itch on his shoulder. He glanced down, making no eye contact, as they approached, and felt a swelling of relief as they passed him. It was shortlived, as they suddenly spun around. The nearest one shoved him hard. He tried to brace himself with his bad leg but it simply wasn’t strong enough, and it buckled under him. He shrieked in fear. They leapt on him, he saw a flash of something sharp, and, in a spasm of pain, felt himself cut, slashed across his cheek and then from behind, on his back. It was over in a second and, as they ran off, leaving him on the ground, the second one yanked painfully on his tail.
As discussed in a number of earlier essays, for nearly twenty years, I have spent my summers studying the behavior and physiology of a population of wild baboons living in the grasslands of East Africa. These are smart animals with pungent, individualistic personalities, living out twenty- to twenty-five-year life spans in large social groups. I’ve been able to experience the shock of mortality in a truncated way with them—watching baboons who used to be terrors of the savannah get hobbled with arthritis, now lagging behind when the troop forages for food, or finding myself shuddering at the weathered state of a male, when he and I were both subadult primates in the 1970s when I began my work. They’ve gotten old on me.
With the graying of some of my troop, I’ve gotten the chance to understand how the quality of their later years reflects the quality of how they lived their lives. What I’ve seen is that elderly male baboons occasionally carry out a behavior that is initially puzzling, inexplicable. The reason why it occurs, as well as who carries it out, contains a lesson, I think, about how the patterns of a lifetime can come home to roost.
As discussed in “The Young and the Reckless,” most Old World primate societies, such as those of baboons, are matrilocal—females spend their entire lives in the troop into which they were born, surrounded with female relatives. Males, on the other hand, tend to leave their “natal” troop around puberty, shipping off to parts unknown, off to make their fortune in a different troop. It is a pattern common to most social species—one of the sexes has to emigrate to avoid inbreeding. And, as discussed in that essay, an odd feature of such transfers among primates is that it is voluntary, unlike in many species where males are forced out by the resident breeding male at their first sign of secondary sexual characteristics, the first sign that they are turning into sexual competitors. Primates leave voluntarily; they get this itch, a profoundly primate wanderlust that makes it feel irresistible to be anywhere that is not the drab familiar home ground. They leave, gradually make their way into a new troop, are peripheral, subordinate, unconnected, and then slowly form connections and grow into adulthood. It is a time of life fraught with danger and potential and fear and excitement.
Occasionally, a prime-aged male baboon will change troops as well. Those cases are purely career moves—some imposing competitor has just seized the number one position in the hierarchy and is likely to be there for a while, a cooperative coalition of males has just unseated you from your own position, some such strategic setback occurs—now is a
n expedient time to try rising on some other troop’s corporate ladder.
But what I and others have seen is that some elderly male primates will also transfer troops. This initially makes little sense, given what aging is about. This is no time of life for an animal to spend alone, unprotected in the savannah, during the limbo period of having left one troop but not yet having been assimilated into another. Senses are less acute, muscles are less willing, and predators lurk everywhere. The mortality risk for a young baboon increases two- to tenfold during the vulnerable transfer period; just imagine what it must be like for an elderly animal.
The Trouble with Testosterone Page 12