How do we humans announce, and excite, sexual availability? Many animals do it with their own biochemical bouquets known as . "Why do bulls and horses turn up their nostrils when excited by love?" Darwin pondered deep in one of his unpublished notebooks. He came to believe that natural selection designed animals to produce two, and only two, types of odors—defensive ones, like the skunk's, and scents for territorial marking and mate attracting, like that exuded by the male musk deer and bottled by perfumers everywhere. The evaluative sniffing that mammals engage in during courtship were clues that scent is the chemical equivalent of the peacock's plumage or the nightingale's song—finery with which to attract mates.

In the following century, a rich array of animal pheromones were documented for seals, boars, rodents, and all manner of other critters. But not for human beings.

Some of Darwin's contemporaries embraced human uniqueness in this regard as evidence of our inevitable ascendance, as if Nature's Plan somehow called for the evolution of a nearly naked two-legged primate with a poor sense of smell to conquer the Earth. The French physician Paul Broca—noting that primates' social olfactory abilities are diminished compared to those of other mammals—asserted that monkeys, apes, and humans represent ascending steps from four-legged sniffing beasts to sight-oriented bipeds.

Monkeys, he argued, have smaller "smell brains" than other mammals, and apes' brains are even smaller than that. Among humans, only the tribal "primitives," Broca wrote, could still attach erotic import to the bodily smells of man.

More enlightened researchers dismissed such views as racist tripe. But they still noted that humans engage in very little scent-driven socializing—compared to, say, the urine-washing displays of monkeys (during which urine is rubbed on the feet to attract mates).

To make matters worse, humans seemed to lack the hardware for communicating by scent. Pheromone reception in other species is the business of two little pits (one in each nostril) known collectively as the vomeronasal organ (VNO). Few scientists of the time claimed to have been able to locate a human VNO. Those who did complained that the VNO is so small that they could detect it only rarely.

But most scientists, without bothering to look, simply dismissed the idea of a VNO in humans. It's been scientific dogma for most of this century that humans do not rely on scent to any appreciable degree, and that any VNOs found are vestigial throwbacks. Then, in the 1930s, physiologists declared that humans lack the brain part to process VNO signals, firmly closing the book on any role for body odor in human sexual attraction. Even if we had a VNO, the thinking was, our brains wouldn't be able to interpret its signals.

Recent discoveries suggest, however, that the reports of our olfactory devolution have been greatly exaggerated.

Some suspected as much the whole time. Smell researchers Barbara Sommerville and David Gee of the University of Leeds in England observed that smelling one another's hands or faces is a nearly universal human greeting. The Eskimo kiss is not just a rubbing of noses but a mutual sniffing. "Only in the Western world," the researchers point out, "has it become modified to a kiss." Hands and faces may be significant choices for these formalities—they are the two most accessible concentrations of scent glands on the human body besides the ears.

Scent And Sentiment

Curiously, remembering a smell is usually difficult—yet when exposed to certain scents, many people—of whom Proust is the paragon—may suddenly recall a distant in emotionally rich detail. Some aromas even affect us physiologically. Laboratory researchers exploring human olfaction have found that:

A faint trace of lemon significantly increases people's perception of their own health.

Lavender incense contributes to a pleasant mood—but it lowers volunteers' mathematical abilities.

A whiff of lavender and eucalyptus increases people's respiratory rate and alertness.

The scent of phenethyl (a constituent of rose oil) reduces blood pressure.

Such findings have led to the rapid development of an aromatherapy industry. Aromatherapists point to scientific findings that smell can dramatically affect our moods as evidence that with aromatic oils can help buyers manage their emotional lives.

Mood is demonstrably affected by scent. But scientists have found that, despite some extravagant industry promises, the attraction value in perfumes resides strictly in their pleasantness, not their sexiness. So far, at least, store-bought scent is more decoration than mood manager or love potion. A subtle "look this way" nudge to the nose, inspiring a stranger's curiosity, or at most a smile, is all perfume advertisers can in good claim for their products—not overwhelming and immediate infatuation.

Grandiose claims for the allure of a bottled smell are not new. In their haste to mass-market sexual attraction during the last century, perfumers nearly drove the gentle musk deer extinct. In Victorian England, a nice-smelling young lady with financial savvy could do a brisk business selling handkerchiefs scented with her body odor.

So it should come as no surprise that when physiologists discovered a functioning vomeronasal organ inside the human nose, it was a venture capitalist intent on cashing in on manufactured human pheromone who funded the team's research. That was in the mid 1980s. Using high-tech microscope probes that were unavailable to VNO hunters earlier in the century, a team led by Luis Monti-Bloch of the University of Utah found a tiny pair of pits, one in each nostril, snuggled up against the septum an inch inside the nose.

The pits are lined with receptor cells that fire like mad when presented with certain substances. Yet subjects report that they don't smell a thing during such experiments. What they often do report is a warm, vague feeling of well-being.

And the olfactory bulb that neurophysiologists couldn't find in the 1930s isn't absent in human brains at all, researchers recently discovered. It's just so enveloped by the massive frontal cortex that it's very difficult to find. This finding, coupled with the discovery of a functional human VNO, has ushered in a new chapter of the story of a human pheromone.

The Great Pheromone Hunt

For an animal whose nose supposedly plays no role in sexual attraction or , human emotions are strongly moved by smells. And we appear to be profoundly overequipped with smell-producing hardware for what little sniffing we have been thought to be up to. Human sweat, urine, breath, saliva, breast milk, skin oils, and sexual secretions all contain scent-communicating chemical compounds. Zoologist Michael Stoddart, author of The Scented Ape (Cambridge University Press, 1991), points out that humans possess denser skin concentrations of scent glands than almost any other mammal. This makes little sense until one abandons the myth that humans pay little to the fragrant or the rancid in their day-to-day lives.

Part of the confusion may be due to the fact that not all smells register in our conscious minds. When those telltale scents were introduced to the VNO of human subjects, they didn't report smelling anything—but nevertheless demonstrated subtle changes in mood.

What could be a source of what might be our very own pheromone?

Humans possess three major types of skin glands—sebaceous glands, eccrine (or sweat) glands, and apocrine glands. Sebaceous glands are most common on the face and forehead but occur around all of the body's openings, including eyelids, ears, nostrils, lips, and nipples. This placement is particularly handy, as the secretions of these glands kill potentially dangerous microorganisms. They also contain fats that keep skin supple and waterproof and, on the downside, cause acne. Little is known, however, about how sebaceous glands contribute to human body odor.

The sweat glands exude water and salt and are non-odorous in healthy people. That leaves the third potential source of a human pheromone—the apocrine gland. Apocrine glands hold special promise as the source of smells that might affect interpersonal interactions. They do not serve any temperature-managing functions in people, as they do in other animals. They occur in dense concentrations on hands, cheeks, scalp, breast areolas, and wherever we possess body hair—and are only functional after , when we begin searching for mates.

Men's apocrine glands are larger than women's, and they secrete most actively during times of nervousness or excitement. Waiting colonies of bacteria turn apocrine secretions into the noxious fumes that keep deodorant makers in business. Hair provides surface area from which apocrine smells can diffuse—part of the reason why hairier men smell particularly pungent. (Is it any coincidence that hair at the arm pit and the genitals sprouts at puberty, when apocrine glands start producing food for our skin bacteria?)

Most promising of all, apocrine glands exude odorous steroids known to illicit sexual behavior in other mammals. Androsterone—a steroid related to the one that nearly doomed the hapless musk deer—is one such substance. Men secrete more androsterone than women do, and most men become unable to detect the stuff right around the time they start producing it themselves—at puberty.

In 1986, the National Geographic Society organized the World Smell Survey to investigate whether people from all cultures experience odor in the same fashion. They distributed over a million scratch-and-sniff cards and questionnaires about subjects' detection and perceptions of intensity of smells, from banana to the sulfur compounds added to natural gas as a warning agent. Included in the survey was the scent of human androsterone.

The steroid itself is not pleasant to smell. Worldwide, those who could smell it rated it second to last in pleasantness—just ahead of the sulfur compounds put in natural gas. A foul-smelling pheromone? It's hardly what scientists expected to find.

Anti-Pheromones?

Despite the poor showing of androsterone in smell ratings, Karl Grammer of Austria's Institute for Human Biology thought it might be the sought-after human pheromone and studied women's reactions to it. He expected to find that women have a strong, favorable reaction to the smell of androsterone around ovulation, when their sense of smell becomes more acute and when they are most likely to conceive. Changes in their bodies' levels around ovulation, Grammer suspected, may change how women react to androsterone's smell.

He found that women's reactions to androsterone indeed change around ovulation—but not in the manner he expected. Instead of attraction, Grammer's ovulating volunteers shrugged their shoulders and reported ambivalence. Androsterone, it seems, offers little hope to men looking for a $19.95 solution to their dating slumps.

Of Mice And Men

The empirical proof of odor's effect on human sexual attraction came out of left field. Medical geneticists studying inheritance rules for the immune system, not smell physiologists, made a series of crucial discoveries that nobody believed were relevant to human mate preferences—at first.

Research on tissue rejection in organ transplant surgery patients led to the discovery that the body recognizes an alien presence (whether a virus or a surgically implanted kidney) because the body's own cells are coated with proteins that our immune system recognizes as "self." But the immune system gets a lot more subtle about recognizing "nonself" intruders. It can recognize specific types of disease organisms, attach protein identifiers to them, and muster antibodies designed specifically for destroying that particular disease. And it can "remember" that particular invader years later, sending out specific antibodies to it.

A segment of our DNA called the major histocompatibility complex (MHC) codes for some of these disease-detecting structures, which function as the immune system's eyes. When a disease is recognized, the immune system's teeth—the killer T cells—are alerted, and they swarm the intruders, smothering them with destructive enzymes.

Unlike many , which have one or two alternative versions (like the genes that code for attached or unattached ear lobes), MHC genes have dozens of alternatives. And unlike earlobe genes, in which the version inherited from one parent dominates so that the version inherited from the other parent is not expressed, MHC genes are "co-dominant." This means that if a lab mouse inherits a version of an MHC gene for resistance to Disease A from its mother and a version lending resistance to Disease B from its father, that mouse will be able to resist both diseases.

When a female mouse is offered two suitors in mate choice trials, she inevitably chooses to mate with the one whose MHC genes least overlap with her own. It turns out that female mice evaluate males' MHC profile by sniffing their urine. The immune system creates scented proteins that are unique to every version of each MHC gene. These immune by-products are excreted from the body with other used-up chemicals, allowing a discerning female to sniff out exactly how closely related to her that other mouse is.

By choosing MHC-dissimilar mates, a female mouse makes sure that she doesn't inbreed. She also secures a survival advantage for her offspring by assuring that they will have a wider range of disease resistance than they would had she mated with her brother.

It's not that she seeks out diverse MHC genes for her young on purpose, of course. Ancestral females who preferred the smell of closely related males were simply outrun through evolutionary time by females who preferred the scent of unrelated sires.

Can You Smell That Smell?

Since humans show little interest in one another's urine, few researchers thought that the story of MHC in rodent attraction could shed light on human interactions. But then someone made an eyebrow-raising discovery: Human volunteers can discriminate between mice that differ genetically only in their MHC. If human noses could detect small differences in the immune systems of mice (mice!) by giving the critters a sniff, excited researchers realized, we may well be able to detect the aromatic by-products of the immune system in human body odor as well!

A team led by Claus Wedekind at the University of Bern in Switzerland decided to see whether MHC differences in men's apocrine gland secretions affected women's ratings on male smells. The team recruited just under 100 college students. Males and females were sought from different schools, to reduce the chances that they knew each other. The men were given untreated cotton T-shirts to wear as they slept alone for two consecutive nights. They were told not to eat spicy foods; not to use deodorants, cologne, or perfumed soaps; and to avoid , drinking, and during the two-day experiment. During the day, their sweaty shirts were kept in sealed plastic containers.

And then came the big smell test. For two weeks prior, women had used a nasal spray to protect the delicate mucous membranes lining the nose. Around the time they were ovulating (when their sense of smell is enhanced), the women were put alone in a room and presented with boxes containing the male volunteers' shirts. First they sniffed a new, unworn shirt to control for the scent of the shirts themselves. Then the women were asked to rate each man's shirt for "sexiness," "pleasantness," and "intensity of smell."

Sexy Genes

It was found, by Wedekind and his team, that how women rate a man's body odor pleasantness and sexiness depends upon how much of their MHC profile is shared. Overall, women prefer those scents exuded by men whose MHC profiles varied the most from their own. Hence, any given man's odor could be pleasingly alluring to one woman, yet an offensive turnoff to another.

Raters said that the smells they preferred reminded them of current or ex-lovers about twice as often as did the smells of men who have MHC profiles similar to their own, suggesting that smell had played a role in past decisions about who to date. MHC-similar men's smells were more often described as being like a brother's or father's body odor... as would be expected if the components of smell being rated are MHC determined.

Somewhat more surprising is that women's evaluations of body odor intensities did not differ between MHC-similar and MHC-dissimilar men. Body scent for MHC-dissimilar men was rated as less sexy and less pleasant the stronger it was, but intensity did not affect the women's already low ratings for MHC-similar men's smells.

That strong odor turned raters off even with MHC-dissimilar men may be due to the fact odor is a useful indicator of disease. From diabetes to viral infection to schizophrenia, unusually sweet or strong body odors are a warning cue that ancestral females in search of good genes for their offspring may have been designed to heed. (In the case of schizophrenia, the issue is confounded—while some do actually have an unusually sweet smell, many suffer from delusions of foul smells emanating from their bodies.)

Nobody yet knows what roles MHC may play in male evaluations of female . Females' superior sense of smell, however, may well be due to their need to more carefully evaluate a potential mates merits—a poor mate choice for male ancestors may have meant as little as a few minutes wasted, whereas a human female's mistake could result in a nine-month-long "morning after" and a child unlikely to survive.

Perfumers who really want to provide that sexy allure to their male customers will apparently need to get a genetic fingerprint of the special someone before they can tailor a scent that she will find attractive. But before men contemplate fooling women in this way, they should consider the possible consequences.

Fooling Mother Nature

The Swiss researchers found that women taking oral contraceptives (which block conception by tricking the body into thinking it's pregnant) reported reversed preferences, liking more the smells that reminded them of home and kin. Since the Pill reverses natural preferences, a woman may feel attracted to men she wouldn't normally notice if she were not on birth control—men who have similar MHC profiles.

The effects of such evolutionary novel mate choices can go well beyond the bewilderment of a wife who stops taking her contraceptive pills and notices her husband's "newly" foul body odor. Couples experiencing difficulty conceiving a child—even after several attempts at tubal embryo transfer—share significantly more of their MHC than do couples who conceive more easily. These couples' is not caused by either partner's , but to an unfortunate combination of otherwise viable genes.

Doctors have known since the mid-1980s that couples suffering repeated spontaneous abortions tend to share more of their MHC than couples for whom pregnancies are carried to term. And even when MHC-similar couples do successfully bring a to term, their babies are often underweight.

The Swiss team believes that MHC-related pregnancy problems in humans are too widespread to be due to inbreeding alone. They argue that in-couple infertility problems are due to strategic, "decisions" made by women bodies to curtail investment in offspring with inferior immune systems—offspring unlikely to have survived to adulthood in the environments of our evolutionary past.

When Broca and other social Darwinists pointed out that "uncivilized races" were more sensitive to body odor, they may have been correct—insofar as Europeans tend to go to greater lengths to perfume and wash away their natural scents. But this is hardly evidence of European superiority over "less evolved" peoples, as Broca insisted. Paying careful attention to the health of others and their suitability as sires to one's offspring in the disease-rich tropics, whose cultures Broca derided, actually makes exceedingly good sense.

Perfume; daily, soapy showers; convenient contraceptive pills—all have their charms. But they also may be short-circuiting our own built-in means of mate choice, adaptations shaped to our unique needs by millions of years of ancestral adversities. The existence of couples who long for children they cannot have indicates that the Western dismissal of body scent is scarcely benign.

Those who find offensive the notion that animal senses play a role in their attraction to a partner need not worry. As the role of smell in human affairs yields to understanding, we see not that we are less human but that our tastes and emotions are far more complex and sophisticated than anyone ever imagined.

How To Smell A Mate

How does body odor affect a woman's sexiness? Scientists don't know for sure, but they do know that a man's allure depends in part on how many immune system genes he shares with a potential mate.

Since it's known that women can detect genetic compatibility by smell—it's not that men can't but that so far no one knows—the onus is on females to sniff out a suitable squire.

Choosing a genetically compatible partner can be difficult it today's perfume rich postindustrial jungle, and getting your immune system genes profiled can be expensive. Before you run to a doctor for blood work to see whether your mate is a suitable match—and sire for your future children—try listening to your nose. (Unfortunately, the sniff test will only work if you're not taking birth control pills.)