3. Forces of Attraction

What is Sexy?

In the last class, we used a bit of art history to explore degrees to which beauty and sexual attractiveness are socially constructed and ways in which they are genetically programmed. We will now explore sexual selection further.

I apologize in advance for the length of the following reading (it is, in fact, the longest assigned reading in this class); however, though it may be long, the effort is well worth it.

Before reading the passage below, I would like for you to first take a look at these videos of birds in courtship:

The Lyre Bird


The Greater Sage Grouse


And on to the reading!

THE PEACOCK'S TALE

The Australian brush turkey builds the best compost heaps in the world. Each male constructs a layered mound of two tons of leaves, twigs, earth, and sand. The mound is just the right size and shape to heat up to the perfect temperature to cook an egg slowly into a chick. Female brush turkeys visit the males' mounds, lay eggs in them, and depart. When the eggs hatch, the young struggle slowly to the surface of the mound, emerging ready to fend for themselves.

To paraphrase Samuel Butler ("a hen is just an egg's way of making another egg"), if the eggs are just the female's way of making another brush turkey, then the mound is just the male's way of making another brush turkey. The mound is almost as precisely a product of his genes as the egg is of hers. Unlike the female, though, the male has a residual uncertainty. How does he know that he is the father of the eggs in the mound? The answer, discovered by Australian scientists, is that he does not know and, in fact. is often not the father. So why does he build vast mounds to raise other males' offspring when the whole point of sexual reproduction is for his genes to find a way into the next generation? It turns out that the female is not allowed to lay an egg in the mound until she has agreed to mate with the male; that is his price for the mound. Her price is that he must then accept an egg. It is a bargain.

But this puts the mound in an entirely different light. From the male's point of view the mound is not, after all, his way of making young brush turkeys. It is his way of attracting female brush turkeys to mate with him. Sure enough, the females select the best mounds, and therefore the best mound makers, when deciding where to lay their eggs. The males sometimes usurp one another's mounds, so the best mound owner may actually be the best mound stealer.

Even if a mediocre mound would do, a female is wise to pick the best so that her sons inherit the mound-building, mound-stealing, and female-attracting qualities of their father. The male brush turkey's mound is both his contribution to child rearing and a solid expression of his courtship.

The story of the brush turkey's mound is a story from the theory of sexual selection, an intricate and surprising collection of insights about the evolution of seduction in animals, which is the subject of this chapter. And, as will become clear in later chapters, much of human nature can be explained by sexual selection.

IS LOVE RATIONAL?

It is sometimes hard even for biologists to remember that sex is merely a genetic joint venture. The process of choosing somebody to have sex with, which used to be known as falling in love, is mysterious, cerebral, and highly selective. We do not regard any and all members of the opposite sex as adequate partners for genetic joint venture. We consciously decide whether to consider people, we fall in love despite ourselves, we entirely fail to fall in love with people who fall in love with us. It is a mightily complicated business.

It is also nonrandom. The urge to have sex is in us because we are all descended from people who had an urge to have sex with each other; those that felt no urge left behind no descendants. A woman who has sex with a man (or vice versa) is running the risk of ending up with a set of genes to partner hers in the next generation. Little wonder that she is prepared to pick those partner genes carefully. Even the most promiscuous woman does not have sex indiscriminately with anyone who comes along.

The goal for every female animal is to find a mate with sufficient genetic quality to make a good husband, a good father, or a good sire. The goal for every male animal is often to find as many wives as possible and sometimes to find good mothers and dams, only rarely to find good wives. In I972, Robert Trivers noticed the reason for this asymmetry, which runs right through the animal kingdom; the rare exceptions to his rule prove why it generally holds. The sex that invests most in rearing the young-by carrying a fetus for nine months in its belly, for example-is the sex that makes the least profit from an extra mating. The sex that invests least has time to spare to seek other mates. Therefore, broadly speaking, males invest less and seek quantity of mates, while females invest more and seek quality of mates.

The result is that males compete for the attention of females, which means that males have a greater opportunity to leave large numbers of offspring than females and a greater risk of not breeding at all. Males act as a kind of genetic sieve: Only the best get to breed, and the constant reproductive extinction of bad males constantly purges bad genes from the population. From time to time it has been suggested that this is the "purpose" of males, but that commits the fallacy of assuming evolution designs what is for the species.

The sieve works better in some species than in others. Elephant seals are so severely sieved that in each generation a handful of males father all the offspring. Male albatrosses are so faithful to single wives that virtually every male that reaches the right age will breed. Nonetheless, it is fair to state that in the matter of choosing mates, males are usually after quantity and females after quality. In the case of a bird such as a peacock, males will go through their ritual courtship display for any passing female; females will mate with only one male, usually the one with the most elaborately decorated tail. Indeed, according to sexual selection theory, it is the female's fault that the male has such a ridiculous tail. Males evolved long tails to charm females. Females evolved the ability to be charmed to be sure of picking the best males.

This chapter is about a kind of Red Queen contest, one resulted in the invention of beauty. In human beings, when all practical criteria for choosing a mate-wealth, health, compatibility, fertility-are ignored, what is left is the apparently arbitrary criterion of beauty. It is much the same in other animals. In species where the females get nothing useful from their mates, they seem to choose on aesthetic criteria alone.

ORNAMENTS AND CHOOSINESS

To put it in human terms, we are asking of animals (as we later will of human beings): Are they marrying for money, for breeding, or for beauty? Sexual selection theory suggests that much of the behavior and some of the appearance of an animal is adapted not to help it survive but to help it acquire the best or the most mates. Sometimes these two-survival and acquiring a mate-are conflicting goals. The idea goes back to Charles Darwin, though his thinking on the matter was uncharacteristically fuzzy. He first touched on the subject in On the Origin of Species but later wrote an entire book about it: The Descent of Man and Selection in Relation to Sex.

Darwin's aim was to suggest that the reason human races differed from one another was that for many generations the women in each race had preferred to mate with men who looked, say, black or white. In other words, at a loss to explain the usefulness of black or white skin, he suspected instead that black women preferred black men and white women preferred white men-and posited this as cause rather than effect. Just as pigeon fanciers could develop breeds by allowing only their favorite strains to reproduce, so animals could do the same to one another through selective mate choice.

His racial theory was almost certainly a red herring,' but the notion of selective mate choice was not. Darwin wondered if selective "breeding" by females was the reason that so many male birds and other animals were gaudy, colorful, and ornamented. Gaudy males seemed a peculiar result of natural selection since it was hard to imagine that gaudiness helped the animal to survive. In fact, it would seem to be quite the reverse: Gaudy males should be more conspicuous to their enemies.

Taking the example of the peacock, with its great tail decked with iridescent eyes, Darwin suggested that peacocks have tails (they are not actually tails but elongated rump feathers that cover the tail) because peahens will mate only with peacocks that have long tails. After all, he observed, peacocks seem to use their tail when courting females. Ever since then the peacock has been the crest, mascot, emblem, and quarry of sexual selection.

Why should peahens like long tails? Darwin could only reply: Because I say so. Peahens prefer long trains, he said, because of an innate aesthetic sense-which is no answer at all. And peahens choose peacocks for their tails rather than vice versa because, sperm being active and eggs passive, that is usually the way of the world: Males seduce, females are seduced.

Of all Darwin's ideas, female choice proved the least persuasive. Naturalists were quite happy to accept the notion that weapons, such as antlers, could have arisen to help males in the battle for females, but they instinctively recoiled at the frivolous idea that a peacock's tail should be there to seduce peahens. They wanted, rightly, to know why females would find long tails sexy and what possible value they could bring the hens. For a century after he proposed it, Darwin's theory of female choice was ignored while biologists tied themselves in furious knots to come up with other explanations. The preference of Darwin's contemporary, Alfred Russel Wallace, was initially that no ornaments, not even the peacock's tail, required any explanation other than that served some useful purpose of camouflage. Later he thought were the simple expression of surplus male vigor. Julian Huxley, who dominated the discussion of the matter for many years, much preferred to believe that almost all ornaments and ritual displays were for intimidating other males. Others believed that the ornaments were aids to females for telling species apart, so that chose a mate of the right species. The naturalist Hugh Cott was so impressed by the bright colors of poisonous insects that he suggested all bright colors and gaudy accessories were about warning predators of dangers. Some are. In the Amazon rain forest the butterflies are color-coded: yellow and black means distasteful, blue and green means too quick to catch. In the 1980s a new version of this theory was adapted to birds, suggesting that colorful birds are the fastest fliers and are flaunting the fact to hawks and other predators: I'm fast, so don't even think of trying to chase me. When a scientist put stuffed male and female pied flycatchers out on perches in a wood, it was the dull females that were attacked first by hawks, not the colorful males.' Any theory, it seemed, was preferred to the idea of female preference for male beauty.

Yet it is impossible to watch peacocks displaying and not come away believing that the tail has something to do with the seduction of peahens. After all, that was how Darwin got the idea in the first place; he knew that the gaudiest plumes of male birds were used in courting females and not in other activities. When two peacocks fight or when one runs away from a predator, the tail is kept carefully folded away.

TO WIN OR TO WOO

It took more than this to establish the fact of female choice. There were plenty of diehards who followed Huxley in thinking courtship was all a matter of competition between males. "Where female choice has been described, it plays an ancillary, and probably less significant, role than competition between males," wrote British biologist Tim Halliday as late as 1983.1° Just as a female red deer accepts her harem master, who has fought for the harem, so perhaps a peahen accepts that she will mate with the champion male.
In one sense the distinction does not matter much. Peahens that all pick the same cock and red deer hinds that indifferently submit to the same harem master both end up "choosing" one male from among many. In any case, the peahens' "choice" may be no more voluntary or conscious than the hinds'. The peahens have merely been seduced rather than won. They may have been seduced by the display of the best male without ever having given the mat-ter a conscious thought-let alone realized that what they were doing was "choosing." Think of human analogies. Two caricatured cavemen who fought to the death so that the winner could sling the loser's wife over his shoulder and take her away are at one extreme; Cyrano de Bergerac, who hoped to seduce Roxanne with words alone, is at the other. But in between there are thousands of permutations. A man can "win" a woman by competing with other men, he can woo her, or both.

The two techniques-wooing and winning-are equally likely to sieve out the "best" male. The difference is that whereas the first technique will select dandies, the second will select bruisers, Thus, bull elephant seals and red deer stags are big, armed, and dangerous. Peacocks and nightingales are aesthetic show-offs.

By the mid-1980s evidence had begun to accumulate that, in many species, females had a large say in the matter of their mating partner. Where males gather on communal display arenas, a male's success owes more to his ability to dance and strut than to his ability to fight other males.

It took a series of ingenious Scandinavians to establish that female birds really do pay attention to male plumes when choosing a mate. Anders Moller, a Danish scientist whose experiments are famously clever and thorough, found that male swallows with artificially lengthened tails acquired mates more quickly, reared more young, and had more adulterous affairs than males of normal length. Jakob Hoglund proved that male great snipe, which display by flashing their white tail feathers at passing females, could be made to lure more females by the simple expedient of having white typing-correction fluid painted onto their tails." The best experiment of all was by Malte Andersson, who studied the widow bird of Africa. Widow birds have thick black tails many times the lengths their bodies, which they flaunt while flying above the grass. Andersson caught thirty-six of these males, cut their tails, and either spliced on a longer set of tail feathers or left them shortened. Those with elongated tails won more mates than those with shortened tails or tails of unchanged length. Tail-lengthening experiments in other species that have unusually long tails have similarly boosted male success.

So females choose. Definitive evidence that the female preference itself is heritable has so far been hard to come by, but it would be odd if it were not. A suggestive hint comes from Trinidad where small fish called guppies vary in color according to the stretch of water they inhabit. Two American scientists proved that in those types of guppies in which the males are brightest orange in color, the females show the strongest preference for orange males.

This female preference for male ornaments can actually be a threat to the survival of the males. The scarlet-tufted malachite sunbird is an iridescent green bird that lives high on the slopes of Mount Kenya where it feeds on the nectar of flowers and on insects that it catches on the wing. The male has two long tail streamers, and females prefer the males with the longest streamers. By lengthening the tail streamers of some males, shortening those of others, adding weight to those of a third group, and merely adding rings of similar weight to the legs of a fourth, two scientists were able to prove that female-preferred tail streamers are a burden to their bearers. The ones with lengthened or weighted tails were worse at catching insects; the ones with shortened tails were better; the ones with only rings on their legs were as good as normal."
Females choose; their choosiness is inherited; they prefer exaggerated ornaments; exaggerated ornaments are a burden to males. That much is now uncontroversial. Thus far Darwin was right.

DESPOTIC FASHIONS

The question Darwin failed to answer was why. Why on earth should females prefer gaudiness in males? Even if the "preference was entirely unconscious and was merely an instinctive response to the superior seduction technique of gaudy males, it was the evolution of the female preference, not the male trait, that was hard to explain.

Sometime during the I970s it began to dawn on people that a perfectly good answer to the question had been available since 1930. Sir Ronald Fisher had suggested then that females need no better reason for preferring long tails than that other females also prefer long tails. At first such logic sounds suspiciously circular, but that is its beauty. Once most females are choosing to mate with some males rather than others and are using tail as the criterion-a big once, granted, but we'll return to that-then any female who bucks the trend and chooses a short-male will have short-tailed sons. (This presumes that they inherit their father's short tail.) All the other females are for long-tailed males, so those short-tailed sons will not have much success. At this point, choosing long-tailed males need more than an arbitrary fashion; it is still despotic. Each peahen is on a treadmill and dare not jump off lest she condemn her sons to celibacy. The result is that the females' arbitrary preferences have saddled the males of their species with ever more grotesque encumbrances. Even when those encumbrances themselves threaten the life of the male, the process can continue-as long as the threat to his life is smaller than the enhancement of his breeding success. In Fisher's words: "The two characteristics affected by such a process, namely plumage development in the male and sexual preference in the female, must thus advance together, and so long as the process is unchecked by severe counter-selection, will advance with ever-increasing speed.

Polygamy, incidentally, is not essential to the argument. Darwin noticed that some monogamous birds have very colorful males: mallards, for example, and blackbirds. He suggested that it would still benefit males to be seductive and so win the first females that are ready to breed, if not the most, and his conjecture has largely been borne out by recent studies. Early-nesting females rear more young than late-nesting ones, and the most vigorous songster or gaudiest dandy tends to catch the early female. In those monogamous species in which both males and females are colorful (such as parrots, puffins, and peewits) there seems to be a sort of mutual selection at work: Males follow a fashion for picking gaudy females and vice versa.

Notice, though, that in the monogamous case the male is choosing as well as seducing. A male tern will present his intended with fish, both to feed her and to prove that he can fish well enough to feed her babies. If he is choosing the earliest female to arrive and she is choosing the best fisherman, they are both employing eminently sensible criteria. It is bizarre even to suggest that choice plays no part in their mating. From terns to peafowl there is a kind of continuum of different criteria. A hen pheasant, for example, who will get no help from a cock in rearing her young, happily chooses to ignore a nearby cock who is unmated to join the harem of a cock who already has several wives. He runs a sort of protection racket within his territory, guarding his females while they feed in exchange for sexual monopoly over them. The best protector is more use to her than a faithful house-husband. A pea-hen, on the other hand, does not even get such protection. The peacock provides her with nothing but sperm.

Yet there is a paradox here. In the tern's case, choosing a poor male is a disastrous decision that will leave her chicks liable to starve. In the hen pheasant's case, choosing the less effective harem defender will apparently leave her inconvenienced. In the peahen's case, picking the poorest male will leave her hardly affected at all. She gets nothing practical from her mate, so it seems there is nothing to be lost. You would expect, therefore, that the choice would be made most carefully by the tern and least carefully by the peahen.

Appearances suggest the exact opposite. Peahens survey several males and take their time over their decision, allowing each to parade his tail to best advantage. What is more, most of the peahens choose the same male. Terns mate with little fuss. Females are the most choosy where the least seems to be at stake."

RUNNING OUT OF GENES

Least at stake? One very important thing is at stake in the peafowl case: a bunch of genes. Genes are the only thing a peahen gets from a peacock, whereas a female tern gets tangible help from the male as well. A tern must demonstrate only paternal proficiency; a peacock must demonstrate that he has the best genes on offer. Peacocks are among the few birds that run a kind of market in seduction techniques, called a "lek," after the Swedish word for play. Some grouse, several birds of paradise and manakins, plus a number of antelope, deer, bats, fish, moths, butterflies, and other also indulge in lekking. A lek is a place where males gather in the breeding season, mark out little territories that are clustered together, and parade their wares for visiting females. The characteristic of the lek is that one or a few males, usually those that display is center, achieve most of the matings. But the central position of a successful male is not the cause of his success so much as its consequence: Other males gather around him.

The sage grouse of the American West has been the best studied of lekking birds. It is an extraordinary experience to drive out to the middle of Wyoming before dawn, stop the car on a featureless plain that looks like every other one, and see it come alive with dancing grouse. Each knows his place; each runs through his routine of inflating the air sacs in his breast and strutting forward, bouncing the fleshy sacs through his feathers for all the world like a dancer at the Folies Bergere. The females wander through this market, and after several days of contemplating the goods on offer, they mate with one of the males. That they are choosing, not being forced to choose, seems obvious: The male does not mount the female until she squats in front of him. Minutes later his job is done and her long and lonely parenthood is beginning. She has received only one thing from her mate-genes-and it looks as if she has tried hard to get the best there were to be had.

Yet the problem of greatest choosiness in the species where choice least matters reappears. A single sage grouse cock may per half of all the matings at one lek; it is not unknown for this top male to mate thirty or more times in a morning. The result is that in the first generation the genetic cream is skimmed from the surface of the population, in the second the cream of the cream, in the third the cream of the cream of the cream, and so on. As any dairy farmer can attest, this is a procedure that quickly becomes pointless. There is just not enough separability in cream to keep taking the thickest layer. It is the same for sage grouse. If I0 percent of the males father the next generation, pretty soon all the females and all the males will be genetically identical, and there will be no point in selecting one male over another because they are all the same. This is known as the "lek paradox," and it is the hurdle that all modern theories of sexual selection attempt to leap. How they do so is the subject of the rest of this chapter.

MONTAGUES AND CAPULETS

It is time to introduce the great dichotomy. Sexual selection theory is split into two warring factions. There is no accepted name for each party; most people call them "Fisher" and "Good-genes." Helena Cronin, who has written a masterful history of the sexual selection debate,; prefers "good-taste" and "good-sense." They are sometimes also known as the "sexy-son" versus the "healthy-offspring" theories.

The Fisher (sexy-son, good-taste advocates are those who insist that the reason peahens prefer beautiful males is that they seek heritable beauty itself to pass on to their sons, so that those sons may in turn attract females. The Good-geners (healthy-offspring, good-sense are those who believe that peahens prefer beautiful males because beauty is a sign of good genetic qualities-disease resistance, vigor, strength-and that the females seek to pass these qualities on to their offspring.

Not all biologists admit to being members of one school or the other. Some insist there can be a reconciliation; others would like to form a third party and cry with Mercutio, "A plague on both your houses." But nonetheless the distinction is as real as the enduring feud between Capulets and Montagues in Romeo and Juliet. This is biological civil war.

The Fisherians derive their ideas mostly from Sir Ronald Fisher's great insight about despotic fashion, and they follow Darwin in thinking the female's preference for gaudiness is arbitrary and without purpose. Their position is that females choose males according to the gaudiness of their colors, the length of their plumes, the virtuosity of their songs, or whatever, because the species is ruled by an arbitrary fashion for preferring beauty that none dares buck. The Good-gene people follow Alfred Russel Wallace (though they do not know it) in arguing that arbitrary and foolish as it may seem for a female to choose a male because his long or his song loud, there is method in her madness. The tail or the song tells each female exactly how good the genes are of each male. The fact that he can sing loudly or grow and look after a long tail proves that he can father healthy and vigorous daughters and sons just as surely as the fishing ability of a tern tells his mate that he can feed a growing family. Ornaments and displays are designed to reveal the quality of genes.

The split between Fisher and Good-genes began to emerge 1970s once the fact of female choice had been established to the satisfaction of most. Those of a theoretical or mathematical bent - the pale, eccentric types umbilically attached to their computers - became Fisherians. Field biologists and naturalists - bearded, besweatered, and booted - gradually found themselves Good-geners."

IS CHOOSING CHEAP?

The First round went to the Fisherians. Fisher's intuition was fed into mathematical models and emerged intact. In the early 1980s three scientists programmed their computers to play an imaginary game of females choosing long-tailed males and bearing sons that had the long tails and daughters that shared the preference of their mothers. The longer the male's tail, the greater his mating success but the smaller his chances of surviving to mate at all. The scientist's key discovery was that there exists a "line of equilibrium" on which the game can stop at any point. On that line the handicap to a female's sons of having a long tail is exactly balanced by the advantage those sons have in attracting a mate.

In other words, the choosier the females, the brighter and more elaborate the male ornaments will be, which is exactly what you find in nature. Sage grouse are elaborately ornamented, and only a few males get chosen; terns are unornamented, and most males win mates.

The models also showed that the process could run away from the line of equilibrium with Fisher's "ever-increasing speed" but only if females vary in their (heritable) preference and if the male's ornament is not much of an encumbrance to him. These are fairly unlikely conditions except early in the process when a new preference and a new trait have just emerged.
But the mathematicians discovered more. It mattered greatly if the process of choosing was costly to females. If in deciding which male to mate with a female wastes time that could be more profitably spent incubating eggs or she exposes herself to the risk of being caught by an eagle, then the line no longer stands. As soon as the species reaches it, and the advantages of long tails are balanced by their disadvantages, there is no net benefit to being choosy, so the costs of choice will drive females into indifference. This looked to be fatal to the whole Fisher idea, and there was brief interest in another version of it (which is known as the "sexy-son" theory) that suggested sexy husbands made bad fathers-a clear cost to being a choosy female.'

Luckily, another mathematical insight came to the rescue. The genes that cause the elaborate ornament or long tail to appear are subject to random mutation. The more elaborate the ornament, the more likely that a random mutation will make the ornament less elaborate, not more. Why? A mutation is a wrench thrown into the genetic works. Throwing a wrench into a simple device, such as a bucket, may not alter its function much, but throwing a wrench into a more complicated device, such as a bicycle, will almost certainly make it less good as a bicycle. Thus, any change in a gene will tend to make the ornament smaller, less symmetrical, or less colorful. This "mutational bias" is sufficient, according to the mathematicians, to make it worth the female's while to choose an ornamented male because it means that any defect in the ornament might otherwise be inherited by the sons; by choosing the most elaborate ornament she is choosing the male with the fewest mutations. The mutational bias is also sufficient, perhaps, to defeat the central conundrum that we set the theories earlier-the fact that if the best genetic cream of the cream is taken off each generation, there will soon be no separability left in the cream. Mutational bias keeps turning some of the cream back into milk.

The result of a decade of mathematical games, then, has been to prove that the Fisherians are not wrong. Arbitrary ornaments can grow elaborate for no other reason than that females discriminate between males and end up following arbitrary fashions; and the more they discriminate, the more elaborate the ornaments become. What Fisher said in 1930 was right, but it left a lot of naturalists unconvinced for two reasons. First, Fisher assumed part of what he set out to prove: That females are already choosy is crucial to the theory. Fisher himself had an answer for this, which was that initially females chose long-tailed males for more utilitarian reasons-for example, that it indicated their superior size or vigor. This is not a foolish idea; after all, even the most monogamous species, in which every male wins a female (such as terns), are choosy. But it is an idea borrowed from the enemy camp. And the geners can reply: "If you admit that our idea works initially, why rule it out later on?"

The second reason is more mundane. Proving that Fisher's runaway selection could happen and the ornament get bigger with ever increasing speed does not prove that it does happen. Computers are not the real world. Nothing could satisfy the naturalists but an experiment, one demonstrating that the sexiness of sons drove the evolution of an ornament.

Such an experiment has never been devised, but those like me, with a bias toward the Fisherians find several lines of argument fairly persuasive. Look around the world and what do you see? You see that the ornaments we are discussing are nothing if not arbitrary. Peacocks have eyes in their train; sage grouse have inflatable air sacs and pointed tails; nightingales have melodies of great variety and no particular pattern; birds of paradise grow bizarre feathers like pennants; bower birds collect blue objects. It is a cacophony of caprice and color. Surely if sexually selected ornaments told a tale of their owner's vigor, they would not be so utterly random.

One other piece of evidence seems to weigh in the balance on the side of Fisher-the phenomenon of copying. If you watch a lek carefully, you see that the females often do not make up their own minds individually; they follow one another. Sage grouse hens are more likely to mate with a cock who has just mated with another hen. In black grouse, which also lek, the cocks tend to mate several times in a row if at all. A stuffed female black grouse (known in this species as a greyhen) placed in a male's territory tends to draw other females to that territory-though not necessarily causing them to mate. In guppy fish, females that have been allowed to see two males, one of which is already courting a female, subsequently prefer that male to the other even if the female that was being courted is no longer present.

Such copying is just what you would expect if Fisher was right because it is fashion-following for its own sake. It hardly matters whether the male chosen is the "best" male; what counts is that he is the most fashionable, as his sons will be. If the Good-geners are right, females should not be so influenced by each other's views. There is even a hint that peahens try to prevent one another from copying, which would also make sense to a follower of Fisher.'° If the goal is to have the sexiest son in the next generation, then one way of doing that is to mate with the sexiest male; a second way is to prevent other females from mating with the sexiest male.

ORNAMENTAL HANDICAPS

If females choose males for the sexiness of their future sons, whY shouldn't they go for other genetic qualities, too? The Good-geners think that beauty has a purpose. Peahens choose genetically superior males in order to have sons and daughters who are equipped to survive as well as equipped to attract mates.

The Good-geners can marshal as much experimental support as the Fisherians. Fruit flies given a free choice of mate produce young that prove tougher in competition with the young of those not allowed to choose. Female sage grouse, black grouse, great snipe, fallow deer, and widow birds all seem to prefer the males on their leks that display most vigorously. If a stuffed greyhen is put on the boundary between two blackcocks dancing grounds, the two males fight over the right to monopolistic necrophilia. The winner is usually the male who is most attractive to females, and he is also more likely to survive the next six months than the other male. This seems to imply that attracting females is not the only thing he is good at; he is also good at surviving." The brighter red a male house finch is, the more popular he is with the females; but he is also a better father-he provides more food for the babies-and will live longer because he is genetically more disease-resistant. By choosing the reddest male on offer, females are fore getting superior survival genes as well as attractiveness genes.

It is hardly surprising to find that the males best at seduction tend to be the best at other things as well; it does not prove that females are seeking good genes for their offspring. They might be avoiding feeble males lest they catch a virus from them. Nor do such observations damage the idea that the most important thing a sexy male can pass on to his sons is his sexiness-the Fisher idea. They merely suggest that he can also pass on other attributes.

Consider, though, the case of Archbold's bowerbird, which lives in New Guinea. As in other bowerbirds, the male builds an elaborate bower of twigs and ferns and therein tries to seduce females. The female inspects the bower and mates with the male if she likes the workmanship and the decorations, which are usually objects of one unusual color. What is peculiar about Archbold's bowerbird is that the best decorations consist of feathers from one particular kind of bird of paradise, known as the King of Saxony. These feathers, which are several times longer than the original owner's body and stem from just above his eye, are like a car's antenna sporting dozens of square blue pennants. Because they are molted once a year, do not grow until the bird of paradise is four years old, and are much in demand among local tribesmen, the plumes must be very hard for the bowerbird to acquire. Once acquired they must be guarded against other jealous male bower birds anxious to steal them for their own bowers. So, in the words of Jared Diamond, a female bowerbird who finds a male that has decorated his bower with King of Saxony plumes knows "that she has located a dominant male who is terrific at finding or stealing rare objects and defeating would-be thieves."

So much for the bowerbird. What about the bird of paradise itself, the rightful owner of the plumes? The fact that he survived long enough to grow plumes, grew longer ones than any other male nearby, and kept them in good condition would be an equally reliable indicator of his genetic quality. But it reminds us of the thing that most puzzled Darwin and got the whole debate started: If the point of the plumes is to indicate his quality, might not the plumes themselves affect his quality? After all, every tribesman in New Guinea is out to get him, and every hawk will find him easier to spot. He may have indicated that he is good at surviving, but his chances of survival are now lower for having the plumes. They are a handicap. How can a system of females choosing males that are good at surviving encumber those males with handicaps to survival?

It is a good question with a paradoxical answer, for which we owe a debt of thanks to Amotz Zahavi, a mercurial Israeli scientist. He saw in 1975 that the more a peacock's tail or a bird of paradise's plumes handicapped the male, the more honest the signal was that he sent the female. She could be assured by the very fact of his survival that the long-tailed male in front of her had been through a trial and passed. He had survived despite being handicapped. The more costly the handicap, the better it was as a signal of his genetic quality; therefore, peacocks' tails would evolve faster if they were handicaps than if they were not. This is the reverse of Fisher's prediction that peacocks' tails should gradually cease evolving once they become severe handicaps.

It is an appealing-and familiar-thought. When a Maasai warrior killed a fierce beast to prove himself to a potential mate, he was running the risk of being killed but was also showing that he had the necessary courage to defend a herd of cattle. Zahavi's "handicap" was only a version of such initiation rituals, yet it was attacked from all sides, and the consensus was that he was wrong.

The most telling argument against it was that the sons would inherit the handicap as well as the good genes, so they would be encumbered to the same degree as they were endowed. They would be no better off than if they were unencumbered and unsexy.

In recent years, however, Zahavi has been vindicated. Mathamatical models proved that he might be right and his critics wrong. His vindicators have added to his theory two subtleties that lend it special relevance to the Good-gene theory of sexual selection. The first is that handicaps might (perhaps must) not only affect survival and reflect quality but also do so in a graduated way; the weaker the male, the harder it would be to produce or maintain a tail of a given length. And indeed, experiments on swallows have shown that birds promoted above their station, by being given longer tail streamers than they grew naturally, could not the next time grow as long a tail as before; carrying the extra handicap had taken its toll. The second is that the handicapping ornament might be designed so as best to reveal deficiency. After all, life would be a lot easier for swans if they were not white, as anybody who has tried swimming in a lake in a wedding dress would know. Swans do not become white until they are a few years old and ready to breed; perhaps being whiter than white proves to a skeptical swan that its suitor can spare the time from feeding to clean his plumage.

The vindication of Zahavi played a critical role in reigniting the debate between Fishererians and Good-geners. Until that happened, Good-gene theories could work only if the ornaments they resulted in were not encumbrances to the males. Thus, a male might advertise the quality of his genes, but to do so at a high cost to himself would be counterproductive unless there were a sexy-son effect.

LOUSY MALES

The handicap theory now comes face-to-face with the central conundrum of sexual selection. This is the lek paradox: that peahens are constantly skimming off the cream of the genetic cream by choosing only the very best males to mate with, and as a result, within very few generations, no variety is left to choose from. The good-gene assertion that mutations are likely to make ornaments and displays less effective provides a partial answer, but it is not a persuasive one. After all, it argues only for not choosing the worst rather than for choosing the best.

Only the Red Queen can solve our dilemma. What sexual selection theory seems to have concluded is that females are con_ stantly running (by being so selective) but are staying in the same place (having no variety to select from). When we find that, we should be on the lookout for some ever-changing enemy, some arms-race rival. It is here that we meet Bill Hamilton again. We last encountered him when discussing the idea that sex itself is an essential part of the battle against disease. If the main purpose of sex is to grant your descendants immunity from parasites, then it follows directly that it makes sense to seek a mate with parasite-resistance genes. AIDS has reminded us all too forcibly of the value of choosing a healthy sexual partner, but similar logic applies to all diseases and parasites. In 1982, Hamilton and a colleague, Marlene Zuk (now at the University of California at Riverside), suggested that parasites might hold the key to the lek paradox and to gaudy colors and peacocks' tails, for parasites and their hosts are continually changing their genetic locks and keys to outwit each other. The more common a particular strain of host is in one generation, the more common the strain of parasite is that can overcome its defenses in the next. And vice versa: Whatever strain of host is most resistant to the prevalent strain of parasite will itself be the prevalent strain of host in the next generation. Thus, the most disease resistant male might often turn out to be the descendant of the least resistant one in a previous generation. The lek paradox is thus solved at a stroke. By choosing the healthiest male in each generation, females will be picking a different set of genes each time and never run out of genetic variety to select from.

The Hamilton-Zuk parasite theory was bold enough but the two scientists did not stop there. They looked up the data for 109 species of bird and found that the most brightly colored species were also the ones most troubled by blood parasites. That claim as been challenged and much debated, but it seems to hold up. Zuk found the same in a survey of 526 tropical birds, and others found it to be true of birds of paradise and some species of freshwater fishg- the more parasites, the showier the species. Even among human beings, the more polygamous a society, the greater its parasite burden, though it is not clear if this means anything. And these might be no more than suggestive coincidences; correlation does not imply cause. Three kinds of evidence are needed to turn their conjecture into a fact: first, that there are regular genetic cycles in hosts and parasites; second, that ornaments are especially good at demonstrating freedom from parasites; third, that females choose the most resistant males for that reason rather than the males just happening to be the most resistant.

The evidence has been pouring in since Hamilton and Zuk first published their theory. Some of it supports them, some does not. None quite meets all the criteria set forth above. Just as the theory predicts that the more flamboyant species should be the ones most troubled by parasites, so it predicts that within a species the more flamboyant a male's ornament, the lower his parasite burden. This proves to be true in diverse cases; it is also true that females generally favor males with fewer parasites. This holds for sage grouse, bowerbirds, frogs, guppies, even crickets. In swallows, females prefer males with longer tails; those males have fewer lice, and their offspring inherit louse resistance even when reared by foster swallow parents. Something similar is suspected in pheasants and jungle fowl (the wild species to which domestic chickens belong. Yet these are deeply unshocking results. It would have been far more surprising to find females being seduced by sick, scrawny males than to find them succumbing to the charms of the healthiest. After all, they might be avoiding a sick male for no better reason than that they do not wish to catch his bug.

Experiments done on sage grouse have begun to satisfy some of the skeptics. Mark Boyce and his colleagues at the University of Wyoming found that male grouse sick with malaria do poorly, and so do males covered with lice. They noticed, too, that the lice were easy to notice because they left spots on the males' inflated air sacs. By painting such spots on a healthy male's sac, Boyce and his colleagues were able to reduce his mating success, If they could go on to show cycles from one resistance gene to another mediated by female choice, they would have given the Good-gene theory a significant boost.

THE SYMMETRY OF BEAUTY

In 1991, Anders Moller and Andrew Pomiankowski stumbled on a possible way of settling the civil war between Fisher and Good-genes: symmetry. It is a well-known developmental accident that animals' bodies are more symmetrical if they were in good condition when growing up, and they are less symmetrical if they were stressed while growing. For example, scorpionflies devdop more symmetrically when fathered by well-fed fathers that could afford to feed their wives. The reason for this is simply the old wrench-in-the-works argument: Making something symmetrical is not easy. If things go wrong, the chances are it will come out asymmerical.

Most body parts, such as wings and beaks, should therefore be most symmetrical when they are just the right size ad be the least symmetrical when stress has left them too small or too large. If Good-geners are right, ornaments should be the most svmmetrical when they are the largest because large ornaments indicate the best genes and the least stress. If Fisherians are right, you would expect no relationship between ornament size and symmetry; if anything, the largest ornaments should be the least symmetrical because they reflect nothing about the owner other than that he can grow the largest ornament.

Moller noticed that, among the swallows he studied, the longest tails of the males were also the most symmetrical. This was quite unlike the pattern of other feathers, such as wings, which obeyed the usual rule: The most symmetrical were the ones closest to the average length. In other words, whereas most feathers show a U-shaped curve of asymmetry against length, tail streamers show a steady upward progression. Since the swallows with the longest tails are the most successful in securing mates, it follows that the most symmetrical tails are also doing better. So Moller cut or elongated the tail feathers of certain males and at the same time enhanced or reduced the symmetry of the tails. Those with longer tails got mates sooner and reared more offspring, but within each class of length, those with enhanced symmetry did better than those with reduced symmetry.

Moller interprets this as unambiguous evidence in favor of Good-genes, for it shows that a condition-dependent trait-symmetry-is sexually selected. He joined forces with Pomiankowski to begin to separate those ornaments that show a correlation between symmetry and size from those that do not-in effect, to separate Good-genes from Fisher. Their initial conclusion was that animals with single ornaments-such as a swallow with a long tail-are Good-geners and show increasing symmetry with increasing size, whereas animals with multiple ornaments-such as a pheasant with its long tail, red facial roses, and colorful feather patterns-are mostly Fisherian, showing no relationship between size and symmetry. Since then, Pomiankowski has returned to the subject from a different angle, arguing that Fisher and many ornaments are likely to predominate when the cost to females of choosing is cheap; Good-genes will predominate when the cost of choosing is high. Again we reach the same conclusion: Peacocks are Fisherian; swallows are Good-geners.

HONEST JUNGLE FOWL
So far I have considered the evolution of male ornaments mainly from the female's point of view because it is her preferences that drive that evolution. But in a species such as a peafowl, where female choice of mate rules, the male is not entirely a passive spectator of his evolutionary fate. He is both an ardent suitor and an eager salesman. He has a product to sell-his genes, perhaps-and information to impart about that product, but he does not simply hand the information over and await the peahen's decision. He is out to persuade her, to seduce her. And just as she is descended from females who made a careful choice, so he is descended from males who made a hard sell.

The analogy of the sales pitch is revealing, for advertisers do not promote their product merely by providing information about it. They fib, exaggerate, and try to associate it with pleasurable images. They sell ice cream using sexy pictures, airplane tickets using couples walking hand in hand on beaches, instant coffee using romance, and cigarettes using cowboys.
When a man wants to seduce a woman, he does not send her a copy of his bank statement but a pearl necklace. He does not send her his doctor's report but lets slip that he runs twenty miles a week and never gets colds. He does not tell her what degree he got but instead dazzles her with wit. He does not display testaments to how thoughtful he is but sends her roses on her birthday. Each gesture has a message: I'm rich, I'm fit, I'm clever, I'm nice. But the information is packaged to be more seductive and more effective, just as the message "Buy my ice cream" catches the eye when it is accompanied by a picture of two good-looking people seducing each other.

In courtship, as in the world of advertising, there is a discrepancy of interests between the buyer and the seller. The female needs to know the truth about the male: his health, wealth, and genes. The male wants to exaggerate the information. The female wants the truth; the male wants to lie. The very word seduction implies trickery and manipulation."
Seduction therefore becomes a classic Red Queen contest, although this time the two protagonists are male and female, not host and disease. Zahavi's handicap theory, as explored by Hamilton and Zuk, predicted that honesty would eventually prevail and males who cheat would be revealed. This is because the handicap is the female's criterion of choice for the very reason that it reveals the male's state of health.

The red jungle fowl is the ancestor of the domestic chicken. Like a farmyard rooster, the cock is equipped with a good many ornaments that his mate does not share: long, curved tail feathers, a bright ruff around the neck, a red comb on the crown of his head, and a loud dawn call, to name the most obvious. Marlene Zuk wanted to find out which of these mattered to female jungle fowl, so she presented sexually receptive hens with two tethered males and examined which they chose. In some of the trials one of the was reared with a roundworm infection in his gut, which affected his plumage, beak, and leg length very little but showed cleary in his comb and eye color, both of which were less colorful than in healthy males. Zuk found that hens preferred cocks with good combs and eyes but paid less attention to plumage. She failed to make hens go for males with fake red elastic combs on their however; they found them too bizarre. Nonetheless, it was clear that hens paid most attention to the most health informative feature of a cock."

Zuk knew that poultry farmers, too, observe the comb and wattles of a cockerel to judge his health. What intrigued her was the idea that the wattles were more "honest" about the state of a than his feathers. Many birds, especially in the pheasant family, grow fleshy structures about their faces to emphasize during display: Turkeys grow long wattles over their beaks, pheasants have fleshy red "roses" on their faces, sage grouse bare their air sacs and tragopans have expandable electric blue bibs beneath their chins.

A cockerel's comb is red because of the carotenoid pigments in it. A male guppy fish is rendered orange by carotenoids also, and a housefinch's and a flamingo's red plumage also depends on carotenoids. The peculiar thing about carotenoids is that birds and fish cannot synthesize them within their own tissues; they extract them from their food - from fruit, shellfish, or other plants and invertebrates. But their ability to extract carotenoids from their food and deliver it to their tissues is greatly affected by certain parasites. A cockerel affected by the bacterial disease coccidiosis, for examples, accumulates less carotenoid in his comb than a healthy cockerel, even when both animals have been fed equal quantities if carotenoid. Nobody knows exactly why the parasites have this specific biochemical effect, but it seems to be unavoidable and is therefore extremely useful to the female: The brightness of carotenoid-filled tissues is a visible sign of the levels of parasite infection. It is not surprising that red and orange are common colors in fleshy ornaments used in display, such as the combs, wattles, and lappets of pheasants and grouse.

The size and brightness of such combs may be affected by parasites, but they are effected by hormones. The higher the level of testosterone in the blood of a cockerel, the bigger and brighter his comb and wattles will be. The problem for the cockerel is that the higher his level of testosterone, the greater his parasite infestation. The hormone itself seems to lower his resistance to parasites." Once again nobody knows why, but cortisol, the "stress" hormone that is released into the bloodstream during times of emotional crisis, also has a marked effect on the immune system. A long study of cortisol levels in children in the West Indies revealed that the children are much more likely to catch an infection shortly after their cortisol levels have been high because of family tension or other stress. Cortisol and testosterone are both steroid hormones, and they have a remarkably similar molecular structure. Of the five biochemical steps needed to make cholesterol into either cortisol or testosterone, only the last two steps are different." There seems to be something about steroid hormones that unavoidably depresses immune defense. This immune effect of testosterone is the reason that men are more susceptible to infectious diseases than women, a trend that occurs throughout the animal kingdom. Eunuchs live longer than other men, and male creatures generally suffer from higher mortality and strain. In a small Australian creature called the marsupial mouse, all the males contract fatal diseases during the frantic breeding season and die. It is as if male animals have a finite sum of energy that they can spend on testosterone or immunity to disease, but not both at the same times'

The implication for sexual selection is that it does not pay to lie. Having sex-hormone levels that are too high increases the size of your ornaments but makes you more vulnerable to parasites, which are revealed in the state of those ornaments. It is possible that it works in the other direction: The immune system suppresses the production of testosterone. In Zuk's words, "Males are thus necessarily more vulnerable to disease as they acquire the accoutrements of maleness."

The best proof of these conjectures comes from a study of roach, which are small fish with reddish fins, in the Lake of Biel in Switzerland. Male roach grow little tubercules all over their bodies during the breeding season, which seem to stimulate females during courtship as the fish rub against each other. The more parasites a male has, the fewer tubercules he grows. It is possible for a zoologist to judge, just from a male's tubercules, whether he is infested with a roundworm or a flatworm. The implication follows: If a zoologist can deduce which parasite is present, a female roach probably can as well. This pattern results from different kinds of sex hormones; one can be raised in concentration only at the expense of leaving the roach vulnerable to one kind of parasite; the other can be raised only at the expense of lowering defenses against another kind of parasite.

If cockerels' wattles and roach tubercules are honest signals, so presumably are songs. A nightingale that can sing loud and long must be in vigorous health, and one that has a large repertoire of different melodies must be experienced or ingenious, or both. An energetic display such as the pas de deux of a pair of male manakins may also be an honest signal. A bird that merely shows its feathers, such as a peacock or a bird of paradise, might be a cheat whose strength has been sapped by bad habits since he grew the plumes. After all, peacock feathers still shine brightly when their owner is dead and stuffed. Perhaps it is no surprise, then, that most male birds do not molt just before the breeding season but adopt their spring plumage the autumn before. They have to keep it tidy all winter. The very fact that a male has looked after his plumes for six months tells a female something about his enduring vigor. Bill Hamilton points out that white fluffy feathers around a bird's rear end, which are common in grouse of various kinds, must especially hard to keep clean if the bird has diarrhea.

Zahavi certainly believed that honesty was a prerequisite of handicaps, and vice versa. To be honest, he thought, an ornament must be costly; otherwise it could be used to cheat. A deer cannot grow large antlers without consuming five times its normal daily intake of calcium; a pupfish cannot be iridescent blue unless it is genuinely in good condition, a fact that will be tested by other male fish in fights. On the assumption that anybody who refuses to play the game and use an honest signal must have something to hide, males are likely to find themselves dragged into honest displays. Therefore, display ornaments are examples of "truth in advertising."

All this is very logical, but in about 1990 it started to make one group of biologists uneasy. They had an instinctive aversion to the idea that sexual advertising is about the truth because they knew that television advertising is not about passing on information; it is about manipulating the viewer. In the same way, they argued, all animal communication is about manipulating the receiver.

The first and most eloquent (manipulative?) champions of this view were two Oxford biologists, Richard Dawkins and John Krebs. According to them, a nightingale does not sing to inform potential mates about himself; he sings to seduce them. If that means lying about his true prowess, so be it. Perhaps an ice cream advertisement is honest in a simplistic sense because it gives the name of the brand, but it is not honest in implying that sex is sure to follow after every spoonful. Such a crude lie can surely be perceived by that genius of the animal kingdom, humans. But it is not. Advertising works. Brand names are better known if they are advertised with sexy or alluring pictures, and better-known brands sell better. Why does it work? Because the price the consumer would have to pay in ignoring the subliminal message is just too high. It is better to be fooled into buying the second-best ice cream than go to the bother of educating yourself to resist the salesmanship.
Any peahens reading this might begin to recognize their dilemma. For they, too, may be fooled by the male's display into buying the second-best male. Remember, the lek paradox argues that there is little to choose between males on a lek anyway because they were all fathered by the same few males in the previous generation. So two theories-truth in advertising and dishonest manipulation-seem to come to opposite conclusions. Truth in advertising concludes that females will discover a cheating seducer; dishonest 'manipulation concludes that males will seduce females against their better judgment.

WHY DO YOUNG WOMEN HAVE NARROW WAISTS?

Marian Dawkins and Tim Guilford of Oxford have recently suggested a resolution to this conundrum. As long as detecting the dishonesty in the signal is costly to the female, it might not be worth her while to do so. In other words, if she has to risk her life seeking out and comparing many males to ensure that she has chosen the best one, then the marginal advantage she gains by picking the best one is outweighed by the risk she has run. It is better to let herself be seduced by a good one than to have the best become the enemy of the good. After all, if she cannot easily distinguish the truthful from the dishonest badge of quality, then other females will not, either, and so her sons will not be punished for any dishonesty they inherit from their father.

A startling example of this sort of logic comes from a controversial theory about human beings that was developed a few years ago by Bobbi Low and her colleagues at the University of Michigan. Low was looking to explain why young women have fat on their breasts and buttocks more than on other parts of their bodies. The reason this requires explaining is that young women are different from other human beings in this respect. Older women, young girls, and men of all ages gain fat on their torsos and limbs much more evenly. If a woman of twenty or so gains weight, it largely takes the form of fat on the breasts and buttocks; her waist can remain remarkably narrow.

So much is undisputed fact. What follows is entirely conjecture, and it was a conjecture that caused Low a good deal of sometimes vicious (and mostly foolish) criticism when she published the idea in 1987.

Twenty-year-old women are in their breeding prime; therefore, the unusual pattern of fat distribution might be expected to be connected with getting a mate or bearing children. Standard explanations concern the bearing of children; for example, fat is inconvenient if it competes for space about the waist with a fetus. Low's explanation concerns the attraction of mates and takes the form of a Red Queen race between males and females. A man looking for a wife is likely to be descended from men who found two things attractive (among many others): big breasts, for feeding his children, and wide hips, for bearing them. Death during infancy due to a mother's milk shortage would have been common before modern affluence-and still is in some parts of the world. Death of the mother and infant from a birth canal that was too narrow must also have been common. Birth complications are peculiarly frequent in humans for the obvious reason that the head size of a baby at birth has been increasing quickly in the past 5 million years. The only way birth canals kept pace (before Julius Caesar's mother was cut open) was through the selective death of narrow-hipped women.

Grant, then, that early men may have preferred women with relatively wide hips and large breasts. That still does not explain the gaining of fat on breasts and hips; fat breasts do not produce more milk than lean ones, and fat hips are no farther apart than lean ones of the same bone structure. Low thinks women who gained fat in those places may have deceived men into thinking they had milkful breasts and wide hip bones. Men fell for it-because the cost of distinguishing fat from heavy breasts or of distinguishing fat from wide hips was just too great, and the opportunity to do so was lacking. Men have counterattacked, evolutionarily speaking, by "demanding" small waists as proof of the fact that there is little subcutaneous fat, but women have easily overcome this by keeping waists slim even while gaining fat elsewhere.'
Low's theory might not be right, as she is the first to admit, but it is no less logical or farfetched than any of its rivals, and for our purposes it serves to demonstrate that a Red Queen race between a dishonest advertiser (in this case, unusually, a female) and a receiver who demands honesty may not always be won by the honesty-demanding gender. It is essential, if Low is right, that fat be cheaper to gain than mammary tissue, just as it is essential, for Dawkins and Guilford, that cheating be cheaper than telling the truth.