Don’t Go There

The evolution of disgust

Earthworms are not dangerous to human health, but they look similar to parasitic worms.

Matt Roth

Eureka moments are what every scientist lives for. I’d been mired in sheaves of data, mostly long transcripts of interviews with women in India, Africa, and Europe about their personal hygiene. I’d been asking them what they did, why they cleaned up after their kids, why they used soap and detergents, why they groomed themselves and tidied their houses, and why they washed their hands, or—more often—why they didn’t. The women found it surprisingly hard to explain their cleaning and preening behavior. Often as not, they said that they felt that they needed to remove things that were “yuck”—the smelly, the clammy, the ugly, or the nasty. But when I asked them to explain why, we got stuck. “They are just yuck!” they would say.

When writing essays on disgust, teenage girls in Lucknow, India, listed, among other things, feces, urine, toilets, sweat, menstrual blood, cut hair, impurities of childbirth, vomit, open wound, saliva, dirty feet, bad breath, nose picking, dirty nails, clothes that have been worn, flies, maggots, lice, mouse in a curry, rats, stray dog, meat, fish, pigs, garbage dump, sick person, beggars, touching someone of lower caste, crowded trains, kissing in public, betrayal. Here are some of the things that Dutch women found revolting: feces, cats, aphids in lettuce, hairs, dogs, pollution, vermin, drug users, vomit, drunkenness, dust, rotten waste, fat people, sweat, badsmelling food, insulting, stickiness, politicians, offal, worms, dirty old men, fishmongers’ hands, flies.

Women in Burkina Faso mentioned feces, dirty latrine, dirty food, diarrhea, flies on food, sores, rubbish in the yard, worms, sexual relations before a child is weaned, smelly drains, dirty clothes, sick people, pigs, vomit. A group of women in Cheshire, in the north of England, included feces, stained kitchen, flies, dog diarrhea, moldy food, drunken louts, vomit, rude people, wounds, foul language, maggots, eating with mouth open, man beating a woman, sweaty person, body parts in jars, cruelty to a horse, stained toilet, cleaning another’s false teeth.

If you compare these, you’ll see that what at first sight looks like a ragbag of unrelated rejecta does, in fact, have themes. All of the lists include bodily wastes and body products. All include bad foods, contaminated objects, and immoral behavior. But, like the women who had participated in these studies, I was also stuck for an explanation. What could possibly account for the fact that such disparate items all occasioned a similar response—a feeling of “eugh!” accompanied by a wish to push them all away, to avoid them, to remove them?

Then came the eureka moment. I’d been asked for advice about a rare disease caused by a lung fluke in Asia. I wasn’t certain how to answer the question, but I knew where to go—to the standard reference work on infectious disease: the American Public Health Association’s Control of Communicable Diseases Manual. I flipped through the index, and suddenly a pattern jumped out at me. Interspersed between diseases such as acanthamebiasis and zygomycosis came familiar words: “contaminated food.” “dog feces,” “flies,” “hairs,” “human feces,” “pigs,” “garbage,” “sexual fluids,” “vomit,” “worms,” and “wounds”—all topics from my disgust lists. There was clearly a pattern here.

Some of the most disgusting bodily products turned out to be the most deadly. Feces are the source of more than twenty gastrointestinal infections, including cholera, typhoid, cryptosporidiosis, rotavirus, and the other stomach bugs that are responsible for three-quarters of a million child deaths a year. Nasal mucus carries the agents of tuberculosis, influenza, measles, leprosy, and the pneumonias that kill even more children annually. Saliva transmits herpes, syphilis, and mumps. Blood carries AIDS; hepatitis B, C, and D; Lassa fever; syphilis; and trypanosomiasis. Sexual fluids transmit chlamydia, herpes, AIDS, gonorrhea, syphilis, and trichomoniasis. Other bodily fluids can pass on impetigo, chicken pox, smallpox, diphtheria, thrush, ringworm, influenza, leprosy, meningitis, and German measles.

The rat carries plague and a variety of interesting parasites such as those that cause arenaviral hemorrhagic fever, Lassa fever, and leptospirosis. Dogs vector rabies. Snails and slugs carry helminthic parasites. Insects such as flies and cockroaches walk around in wastes, spreading the agents of gastrointestinal infection. Other insects, like the louse and the scabies mite, are themselves parasites. Some insects are both parasites and parasite vectors at the same time: fleas carry plague and typhus, lice carry relapsing and trench fever, ticks carry encephalitis, Lyme disease, and a variety of viral fevers. Earthworms are not dangerous to human health, but they look similar to the parasitic worms that can be found in meat and fish and that infect more than a third of humanity.

It seemed that I had stumbled on an explanation for the diversity of the disgusting. All of the things that people find revolting seemed to have some sort of role to play in the transmission of infectious disease. A few authors had noted that there might be a connection between disgust and disease but none had explored the idea seriously. Eureka? Almost—only one problem remained. Why did cruelty, rudeness, drunkenness, and politicians appear on my lists of the disgusting? Moral disgust seemed to need a different explanation. I decided to put that problem aside for the time being and explore the role of disgust in protecting us from infectious disease.

Charles Darwin, in The Expression of the Emotions in Man and Animals, included a figure in which the photographer, Oscar Gustave Rejlander, posing as his own model, simulated the expression of disgust. “As the sensation of disgust primarily arises in connection with the act of eating or tasting,” wrote Darwin, “it is natural that its expression should consist chiefly in movements round the mouth. But as disgust also causes annoyance, it is generally accompanied by a frown, and often by gestures as if to push away or to guard oneself against the offensive object.”

Reproduced with permission from John van Wyhe ed., The Complete Work of Charles Darwin Online (http://darwin-online.org.uk)
Like any scientist with a hypothesis, I needed to test it with more data. Where better than the international departure lounge of Athens airport? A student of mine asked more than 250 people from Europe, the Middle East, the United States, and Africa
about what they found disgusting. Setting aside again the rather interesting moral violations (politicians and Americans got the highest disgust scores in this sample), the pattern held up. Bodily fluids and wastes appeared, as well as foods that were spoiled; the insect, bird, and animal vectors of disease; and poor hygiene, all of which are implicated, directly or indirectly, in infectious-disease transmission.

So was born the parasite avoidance theory of disgust (or PAT for short). The reason we recoil when we meet the nasty, the foul, and the stinky is ancient and instinctual. It’s not a reasoned response to “knowing” about germs and disease; rather, it comes from an ancient wellspring of wisdom: the process of evolution. Those of our distant ancestors who tended to avoid feces, nasal mucus, and bad-smelling food did better on average in the reproduction lottery; they were healthier, mated more often, brought up more children to sexual maturity, and hence had more grandchildren. And these grandchildren were more disgustable themselves—and so on down to the present day, and us. Pathogens and parasites caused the evolution of defense systems. These included not just impermeable skin, and internal immune systems to kill parasites once they had gotten inside the body, but also behavioral defenses. Disgust is a voice in our heads, the voice of our ancestors telling us to stay away from what might be bad for us.

It seemed that PAT was right! But, for a scientist, a theory has to be able to be tested to destruction; it has to lead to predictions that can be falsified. Just as we’d published a paper setting out PAT, the BBC came knocking wanting to make a documentary about human instincts. They offered us the chance to carry out a web-based test of the disgust reactions of the good viewers of Britain and others around the world.

We hurriedly pulled together an experiment. The idea was to offer people pairs of photos that were broadly similar, but one of the images would be morphed to enhance the infection content. So we took towels and stained them with food coloring. In one version the stain was blue, in the other the stain was brownish yellow—looking like bodily fluids. Another pair of pictures showed an empty subway train and the same car full of people. We mixed all the photos up and then asked people to rate them for disgust on a sliding scale from 1 to 5. When the survey went live on the night of the broadcast, the response crashed the BBC’s server. In the end more than 160,000 people from 165 countries completed it. Every disease-relevant image scored significantly higher than the less disease-relevant image, and this effect held for every region of the world.

One final test involved a large picture of a toothbrush and a question: whom would you least like to share a toothbrush with: your partner, the weatherman, your boss, your best friend, or the mailman? We predicted that the people who were least personally known would be most likely to carry diseases that had not already been caught, so the weatherman’s brush would be the most aversive, and one’s partner’s toothbrush the least. We got the order right, except for one detail. Sharing the mailman’s toothbrush was most aversive; the weatherman’s came third. On further reflection this made sense, as people probably feel that they know their weatherman, since he is welcomed into the home every evening on TV, while they mostly don’t know their roving mailman.

Our study led to a flurry of press interest and brought me PhD student Mícheál de Barra. He decided that we needed to go back to square one, to use the sharp knives of both epidemiology and evolutionary biology to dissect disgust and look for its joints. We asked ourselves what kinds of places and things it might have been adaptive to avoid, so as to not get invaded by parasites. How should the brain carve up the world of the disgusting? Is it just a jumble of the nasty and the infectious, or does the brain recognize a structure in it?

An infectious-disease textbook became the source of a varied list of sixty situations in which people might risk contracting an infection. We set up a website survey and advertised it on Facebook, getting more than 2,500 people to record how disgusting they found our scenarios. The responses tended to cluster together, and they did so in ways that were subtly different from what we had anticipated.

We had thought that the shape of the disgust response might reflect the routes of entry of pathogens into the body: that there might be a different type of response to the parasitic organisms that we might breathe in, that we ate, that entered through the genital tract, and that got in through the skin, because each of these would require a different kind of behavioral defense, with distinct kinds of mental machinery. But the picture that emerged wasn’t quite like that. We identified six categories of stimuli: people of unusual appearance who showed signs of sickness or deformity; infected lesions and bodily fluids; people with signs of poor hygiene; having risky sex; unfamiliar and possibly infected foods, as well as certain animals and insects; and finally, things in the environment that had come into contact with infectious agents (known as fomites, these are surfaces that vector infection).

While it wasn’t exactly what we were expecting, this pattern still made sense. If you are an animal that cannot directly see infectious agents, then you need to be able to avoid the places and things that tend to harbor pathogens. Since other people are the prime source of human pathogens, avoiding people whose appearance or behavior hints that they might have a disease is paramount. Any bodily substances that they exude should also be dubious, especially if these look or smell infective. People who behave unhygienically—who appear unkempt and poorly groomed or who cause contamination of the shared environment—are also the object of a separate kind of disgust. It’s important to avoid the sorts of contacts with other people that might give you a sexually transmitted disease (as well as avoiding unsuitable mates). Animals and insects that vector disease, as well as foods that are unfamiliar or that show signs of being rotten, are best avoided because they are likely to carry pathogens. Finally, the data suggested that we also have a kind of disgust that is reserved for objects that have come into contact with things that are contaminated (this reaction, possibly unique to humans, is not dependent on knowledge of a germ theory of disease, but rather stems from our ability to remember a sequence of events).

Cartoon from Punch, 1850: The poor quality of London water, especially that of the disease-carrying River Thames, was a recurring topic of satire.

c12261-05/©The British Library Board. All Rights Reserved 11/20/2013

If PAT does explain most human disgust, however, why isn’t it standard wisdom? Historically, it was often thought that our aversions were simply products of culture. More recently, studies of disgust have been dominated by a few famous psychologists, whose model has gone unchallenged.

One of the earliest writers on disgust was Charles Darwin. On his visit to Tierra del Fuego on the Beagle in 1832, he collected observations of interesting human behavior alongside his other specimens. As he recounted in The Expression of the Emotions in Man and Animals (1872), “a native touched with his finger some cold preserved meat which I was eating at our bivouac, and plainly showed utter disgust at its softness; whilst I felt utter disgust at my food being touched by a naked savage, though his hands did not appear dirty.”

From the safety and comfort of Down House, Darwin sent out letters to his global collection of correspondents. They confirmed that the disgust face—turning up the nose, wrinkling the mouth, and making as if to spit, as well as the emission of an “eugh!” sound—was common to Greenlanders, Native Americans, Malays, and Australians. Darwin even recorded the same face in his own infant son. Based on the etymology of the word dégoût, however, Darwin proposed that disgust’s original purpose was the avoidance of things offensive to the taste. This idea that disgust has oral origins has become orthodox. Yet if PAT is right, then disgust must be older than humans and serve to defend all of the portals of the body—the skin, the airways, the genitals—from infection, not just the mouth.

While Darwin emphasized the universality of the emotion, the philosopher Herbert Spencer was one of the earliest to focus on the differences between what different cultures found disgusting: “Here human flesh is abhorred, and there regarded as the greatest delicacy; in this country roots are allowed to putrefy before they are eaten, and in that the taint of decay produces disgust: the whale’s blubber which one race devours with avidity, will in another by its very odor produce nausea.”

Anthropologists from Spencer’s time onward made the differing taboos and prohibitions of different cultures the stock of their trade. The social anthropologist Mary Douglas entrenched this view in her book Purity and Danger: An Analysis of Concepts of Pollution and Taboo, which appeared to great success in the 1960s. She suggested that objects and events that do not fit the local cosmology have to be rejected, and classed as dirty or impure, as otherwise they would pose a threat to the social order. The caste system in India was Douglas’s paradigm case. Human wastes are anomalous materials, neither alive nor dead, both belonging to and rejected by the person. Hence wastes such as feces are dirty and polluting, and humans who deal in them become symbolically impure. Those castes then have to be kept apart, for fear of social disorder.

For Sigmund Freud disgust was a mode of repressing desire. In an essay on sexuality dating from 1902, he proposed that disgust served to defend the brain against its own baser tendencies. For example, learning disgust for feces during toilet training suppresses any temptation to want to contact or eat them.

As a practicing psychiatrist in 1940s America, Andres Angyal found a pattern of disgust objects being “mean and base . . . capable of permeating permanently everything with which they had once come into contact,” leaving “a lingering, unpleasant, after-sensation on the skin even after washing the hands.” From anthropological accounts, he concluded that disgust is more universal than culturally specific. However, the nearest he came to a coherent explanation of the patterns he described was that wastes belong outside and it would be a perversion of nature for them to be taken back in.

Angyal’s analysis was a foundation for the work of Paul Rozin, of the University of Pennsylvania, whose body of work, in later years with New York University social psychologist Jonathan Haidt, has become the gold standard in the literature over the past two decades. In their account disgust has oral origins, arising variously from a distaste for toxins, an evolved aversion to pathogens, and a fear of eating animals. The concern about animals, they say, comes from a magical folk belief that we might become what we eat. That fear has since spread beyond the mouth to the rest of the body. Hence, inappropriate sexual acts, poor hygiene, death, and violations of the ideal body “envelope” or exterior form (e.g. gore, deformity, obesity) are also found disgusting. Their model of disgust also includes interpersonal disgust, which they say serves to protect the body, the soul, and the social order; and moral disgust.

While these works are fascinating and illuminating, all give short shrift to biological explanations. An increasing number of scientists—including Daniel M. T. Fessler, Debra Lieberman, Joshua M. Tybur, Mark Schaller, Richard J. Stevenson, and my group—are exploring disgust from a modern evolutionary perspective. For us, there is a simple and parsimonious solution to the puzzle: although disgust has some cultural variation, as one would expect from an evolved adaptive system, disgust has one central concern. It evolved to defend animals from attack by parasites, the tiny, usually invisible, predators that attack by stealth and eat their hosts alive. It is a brain system that coordinates behavior in the direction of pathogen avoidance—whether the pathogens are in the environment, in other animals, or, especially, in other humans. No magical folk belief, Freudian repression, or existential denial of death is needed to explain disgust.

Reprinted with permission from Don’t Look, Don’t Touch, Don’t Eat: The Science Behind Revulsion, by Valerie Curtis, published by the University of Chicago Press. © 2013 by The University of Chicago. All rights reserved.

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