by Carl Sagan
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Bulls, stallions, and roosters are made into steers, geldings, and capons because humans find their machismo inconvenient—the very same male spirit that the castrators likely admire in themselves. One or two skilled motions of the blade—or a deft bite by a reindeer-herding Lapp woman—and the testosterone levels are down to manageable proportions for the rest of the animal’s life. Humans want their domestic animals to be submissive, easily controlled. Intact males are an awkward necessity; we want just enough of them to father a new generation of captives.
Something similar although less direct happens within the dominance hierarchy. From pit vipers to primates, the loser in ritual combat often experiences a steep decline in testosterone and related sex hormones, making him less likely to challenge the leadership at a later time, and therefore less likely to be injured. On a molecular level, he’s learned his lesson. With fewer circulating steroids, he’s now less ardent in his pursuit of females—at least when high-ranking males are around. This also is to the liking of the alphas. Again, decreases in testosterone levels following defeat are usually much more marked than any increases following victory.
Back to the testicles of sparrows: In a breeding area each little piece of territory has a male sparrow who will defend it against all comers.* Suppose a meddling ornithologist captures one of these territorial males and removes him from the territory. What happens? Other males from adjacent areas—many of them not previously able to defend a territory—move in. Of course they have to threaten and intimidate before they’ll be taken seriously. So the general level of sparrow anxiety rises, both among the newcomers and among unreplaced sparrows in adjacent territories. Political tensions become high. If now we monitor the bloodstreams of the sparrows in the course of their disputes (which from our point of view, of course, seem petty, but to them it’s Quemoy and Matsu), we find that everyone’s testosterone level has risen—the newly introduced males who are trying to establish their territories, and the males of neighboring territories who are now required to do more in the way of defending than has been their recent practice. Something similar is true for many animals.
Those who have more testosterone, by and large, become more aggressive. Those who need more testosterone, by and large, generate it. Testosterone seems to play a vital role as both the cause and the effect of aggression, territoriality, dominance, and the rest of the “boys-will-be-boys” constellation of male behavioral traits. This seems to be true for widely differing species, including monkeys, apes, and humans.
In springtime, stimulated by the increasing day length, the testosterone level in male perching birds and songbirds (such as jays, warblers, and sparrows) goes up; they develop plumage, unveil a scrappy temperament, and begin singing. Males with larger repertoires breed earlier and produce more chicks. The repertoires of the most attractive males range up to dozens of distinguishable songs. Musical variety is the means by which more testosterone is converted into more birds.
When eggs are being laid, the male testosterone level remains high; they’re protecting their mates. Once the females begin incubating the eggs and are uninterested in sexual advances, male testosterone levels fall. Suppose that the females are now given estrogen implants so they remain sexually alluring and receptive, despite their new maternal duties. Then the testosterone levels in the males remain high. As long as the female is sexually available, the male is inclined to be nearby and protective.17
These experiments suggest that an important selective advantage may accrue if a species breaks out of the estrus constraint. Continuous female sexual receptivity keeps the male around for all sorts of useful services. This is just what seems to have happened—maybe through a small adjustment in the DNA code for the internal estrogen clock—in our species.
Testosterone-induced behavior must be subject to limits and constraints. If it were carried to counterproductive lengths, natural selection would quickly readjust the concentration of steroids in the blood. Testosterone poisoning to the point of maladaptation must be very rare. In nectar-eating birds, bats, and insects it’s possible to compare the energy expended in male steroid-driven defense against poachers with the energy that could be extracted from the flowers being guarded.* In fact, territoriality typically turns on only when the energy benefit exceeds the energy cost, only when there are so few delectable flowers to suck that it pays for you to expend the effort to chase away the competition. Nectar-eaters are not rigid territorialists. They won’t fight all comers to protect a wasteland of stones. They make a cost-benefit analysis. Even in a rich garden of nectar-bearing flowers, often no territorial behavior is seen in the morning—because plentiful nectar has been accumulating at night when the birds were asleep. In the morning, there’s enough to go around. Toward noon, when birds from far and wide have been feeding and the resource begins to get scarce, territoriality turns on.18 Wings outstretched, beaks lunging, the locals drive away the intruders. Maybe they feel they’ve been nice guys long enough, but now they’ve had it up to here with these foreigners. Fundamentally, though, it’s an economic, not a patriotic decision; practical, not ideological.
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Many animals may do it, but at least among rats and mice it’s well-demonstrated: Fear is accompanied by a characteristic odor, a fear pheromone, easily recognized by others.19 Often, as soon as they sense you’re afraid, your friends and relatives run away—useful for them, but not very helpful for you. It may even encourage the rival or predator who has prompted your fear in the first place.
In the heads of goslings and ducklings and chicks at the moment they peck their way out of the egg is, a classic experiment suggests, a rough knowledge of what a hawk looks like. No one has to teach it to them. Hatchlings know. They also know fear. Scientists make a very simple silhouette—cut out of cardboard, say: There are two projections which could be wings. They flank a body which is longer and rounded at one end and shorter and stumpy at the other. If the silhouette moves with the long projection first, it looks like a flying goose, wings spread, long neck preceding. Move the silhouette overhead, neck first, over the hatchlings and they go about their business. Who’s scared of a goose? Now move the same silhouette stumpy end first—so it looks like a hawk with wings outstretched and long tail trailing—and there’s a flurry of peeps and trepidation. If this experiment has been properly interpreted,20 somehow, inside the sperm and the egg that made that chick, encoded in the ACGT sequence of their nucleic acids, there’s a picture of a hawk.
Perhaps this inborn fear of raptors is akin to the fear of “monsters” that almost all babies manifest around the time they become toddlers. Many predators who are circumspect when a human adult is around would happily attack a toddler. Hyenas, wolves, and large cats are only a few of the predators that stalked early humans and their immediate ancestors. When the child begins to amble off on its own, it helps for it to know—in its marrow—that there are monsters out there. With such knowledge, it’s much more likely to come running home to the grown-ups at the slightest sign of danger. Any mild predisposition in this direction will be resoundingly amplified by selection.*
In grown-up chickens there’s a set of more organized and systematic responses, including specific auditory alarm calls that alert every chicken within hailing distance of the ominous news: A hawk is overhead. The cry announcing an aerial predator is distinctly different from that announcing a ground predator—a fox, say, or a raccoon. Since the bird sounding the alarm is also giving away its presence and location to the hawk, we might be tempted to consider it courageous, its behavior evolved through group selection. An individual selectionist might argue—how convincingly is another matter—that the cry works to stir other chickens into motion, whose scurrying might distract the hawk and save the bird that sounded the alarm.
Experiments by the biologist Peter Marler and his colleagues21 show that, at least among cockerels, a propensity to make alarm calls depends very much on whether there’s a companion nearby. With no o
ther bird present, the cockerel may freeze or gaze up into the sky when seeing something like a hawk, but he doesn’t cry out in alarm. He’s more likely to sound the alarm if there’s another bird within earshot; and, significantly, he’s much more likely to cry out if his companion is another chicken—any chicken—rather than, say, a bobwhite. He’s indifferent to plumage, though; chickens with very different color patterns are worthy of being warned. All that counts is that the companion be another domestic fowl. Maybe this is just sloppy kin selection, but it certainly edges toward species solidarity.
So is this heroism? Does the cockerel understand the danger he subjects himself to, and then, despite his fear, bravely cry out? Or is it more likely that squawking when there’s a companion nearby but not when you’re alone is a program in the DNA, and nothing more? See a hawk, see another chicken, cry out, and no agonizing moral struggle. When one of the combatants in a cockfight continues, although bleeding and blinded, to fight to the death, is he displaying “invincible courage” (as an English admirer of cockfighting has described it), or is this just a combat algorithm gotten out of hand, escaping the inhibition subroutines? Indeed, in humans does the hero have a lucid grasp of the danger, or is he or she merely following one of our preprogrammed subroutines? Most heroes report that they just did what came naturally, without much conscious thought.
The two sexes are not equally likely to produce alarm calls. In another study by Peter Marler and his colleagues,22 cockerels cried out in alarm every time a hawk silhouette was presented; but hens made such calls only 13% of the time.* Castrated cockerels are much less likely to sound the alarm—except when they have testosterone implants, in which case the call rate goes back up. So testosterone plays a role not just in dominance hierarchies, sex, territoriality, and aggression, but also in providing early warning of predators, whether we hold the bearer to be hero or automaton.
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Preadolescent female mice have a molecule in theirurine that induces testosterone production in males who get a whiff. In turn, the males’ urine now contains pheromones which, when sniffed by the immature female, quicken her sexual development. She matures early if there are males around, and late if there aren’t—a positive feedback loop that saves unnecessary effort. (As you might expect, female mice who can’t detect odors never come into heat.) What’s more, normal pregnant females who sniff the urine from males of a different strain of mice spontaneously abort their pregnancies; they resorb the embryos back into their bodies and quickly come into heat.23 This is convenient for the alien males. If the resident males don’t like it, it’s up to them to stop strangers from coming around with their abortion-inducing aromas.
In mice, as for many other animals, testosterone begins to be manufactured in earnest at puberty, and that’s when serious aggression against other mice begins. In adult males, the more testosterone, the quicker will be the attack when a strange male appears at the territorial frontiers. Again, castrate the males and their aggressiveness declines. Again, deliver testosterone to the castrates and their aggressiveness increases. Male mice are given to “marking” their environment with tiny dribbles of urine—a practice they pursue with redoubled effort when other mice are around (or when they come upon some unfamiliar object, maybe a hairbrush). Because of embryo resorption, if the males are to leave progeny at all, they must be the chief urinators in their territory. Maybe marking is like nametags on luggage, “no trespassing” signs on private property, or heroic portraits of the national leader in public places. The doughty little mouse is singing “This land is my land” and “She belongs to me.” Even when he’s not physically present he wants passersby to take careful note of his proprietorship. As you might suspect, castrate the mouse and urinary marking declines strikingly; resupply testosterone and his compulsion to mark is rekindled.
Normal female mice are infrequent urinators. They are not inveterate markers. But what happens if anatomically normal female infants are jolted with testosterone? Then they begin marking often. (If a similar experiment is done in dogs, adult females who were given testosterone before birth adopt the urination posture of the males; they lift one leg and trickle the urine down the other—one more indignity visited at the hands of the scientists.) When female rats with ovaries surgically removed are supplied with testosterone, they become aggressive, alternating a masculine propensity for confrontation with distinctly feminine sexual behavior. But one thing about giving testosterone to normal females early in their lives: When they grow up, the males find them much less attractive.
While testosterone in the blood is intimately connected with the expression of aggression in male animals, it is by no means the whole story. There are, for example, molecules in the brain that repress aggression. Hereditary strains of rats that are unusually violent turn out to have less of these inhibitory brain chemicals than more peace-loving strains. Aggressive rats are calmed when there are more of these chemicals in their brains; peaceful rats are agitated when there is less of these chemicals. If you’re a rat, busy watching violence in other rats—mice-killing, say—your level of inhibiting brain chemicals drops.24 You’re now more likely to be violent yourself, and not just toward mice. Your repressed aggressive tendencies have been disinhibited. And everybody else’s. Hostility can then rapidly spread through your group, expressed differently by different individuals. Perhaps that’s what happened with Calhoun’s rats, so confined that aggression and despair spread in waves, reflected and amplified from multiple foci through the community. Violence is contagious.
In experiments performed by Heidi Swanson and Richard Schuster,25 rats were given a complex cooperative task to learn, having to run together over specific floor panels in a particular sequence. If they succeeded, they were rewarded with sugar water; if they didn’t, they found themselves racing around the experimental chamber for the fun of it. Nobody taught them what to do, or at least not directly. It was trial and error. The experiment was tried on pairs of males, pairs of females, pairs of castrated males, and pairs of castrated males with testosterone implants. Some of the rats had previously lived alone.
Here’s how it turned out: Females, as well as male castrates, learned fairly quickly. Normal males and castrates with administered testosterone learned much more slowly. Males who had previously lived alone did still worse. Some pairs of previously solitary male rats—pairs with intact testicles as well as pairs of testosterone-jolted castrates—never learned at all.
For the solitary males this is just what you might expect: Because you live alone you have little experience in cooperating, so probably you’re not going to do very well on a demanding test of cooperation. But then, why should females who’ve been living alone be able to figure it out? The answer seems to be that if you’re a solitary male, a loner, and you have to perform a complex task in coordination with someone else, testosterone makes you stupid. Every pair of males who ordinarily lived alone and couldn’t figure out how to pass the test was engaged in violent combat. Communal living, by contrast, tended to calm them down.
Swanson and Schuster conclude that the learning deficits were not so much due to aggression per se, as to aggression in the context of the dominance hierarchy. Those who tended to be the winners in ritualized (or real) combat—almost always it was the same individuals—would strut and saunter with hair erect, threatening, feinting, and occasionally attacking. The subordinates would crouch, close their eyes, and either freeze for long periods or hide. But tendencies to strut or crouch or hide are not well suited for the gymnastic cooperation needed to get that sugar water.
Cooperation has strong democratic overtones. Extreme dominance/submission hierarchies do not. The two are strongly incompatible. In these experiments, females intimidated others and fought as did the males, but today’s winner was often yesterday’s loser, and vice versa—unlike the males. Cowering and freezing were less common, and the female style of aggression didn’t impede social performance as much as her male counterpart’s.
; The unfolding richness and complexity of testosterone-induced sexual behavior—dominance, territoriality and all the rest—is one means by which males compete to leave more offspring. It’s not the only possibility. We’ve already mentioned selection at the level of competition among sperm cells, as well as those species in which the male leaves a vaginal plug when he’s done to frustrate those who come after him. Male dragonflies attempt to undo the competition retroactively: Projecting from the male’s penis is a whip-like prong that attaches itself to the mass of sperm previously deposited in the female. When he withdraws, he takes his rivals’ semen with him. How much more direct the dragonflies are than the birds and mammals—our males violent, consumed with jealousy, spitting out threats and accusations, longing for exclusive sexual access to at least one female. The dragonfly male is spared much of this; he merely rewrites his mate’s sexual history.
We’ve concentrated on aggression, dominance, and testosterone because they seem to be of central importance in understanding human behavior and social systems. But there are many other behavior-eliciting hormones fundamental for human well-being, including estrogen and progesterone in females. The fact that complex behavioral patterns can be triggered by a tiny concentration of molecules coursing through the bloodstream, and that different animals of the same species generate different amounts of these hormones, is something worth thinking about when it’s time to judge such matters as free will, individual responsibility, and law and order.
Had Poseidon more carefully measured out whatever it was he gave to Caenis, the matter would not have come to Zeus’ attention. Had Poseidon’s own testosterone titer been lower, or had there been enforceable penalties against gods raping humans, Caenis might have lived a happy and blameless life. As it was, Caeneus was afflicted by hubris, surely; but only because of the rape and its aftermath. He was guilty of disrespect for the gods, but the gods had shown disrespect for her. There is not a hint that the piety of Thessaly would have been troubled had Poseidon left Caenis alone. She had been minding her own business, walking along the beach.