In 1927 Aurel Kolnai wrote the first scholarly work devoted entirely to the subject of disgust.23 Using the phenomenological approach of self-examination that was current at the time in Austro-Germany, he provided a careful account of his experience of the emotion. For him, biological disgusts included excreta, secreta, dirt, animals, and insects—especially crawling ones—certain foods, the human body in too close contact, exaggerated fertility, disease, and deformity. His moral disgusts included excess and satiety, lies, deceit and corruption, moral weakness, and sentimentality. But Kolnai’s explanation was in the Freudian tradition. Disgust serves a balancing, psychodynamic function, in promoting the avoidance of excess, surfeit, and a desire for death.
As a practicing psychiatrist in 1940s America, Andres Angyal puzzled over the things his patients found disgusting. He found a pattern of disgust objects being “base or mean, capable of permanently permeating anything they have contacted, leaving a lingering, unpleasant after-sensation, even after washing the hands.”24 For Angyal, disgust objects often had a sense of the uncanny—being cold and clammy and implying death. From anthropological accounts, he concluded that disgust is more universal than culturally specific, and that it operates independently of any knowledge about disease or microbes. 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, who could be called the “father of disgust.” His body of work, later with his collaborator Jonathan Haidt, is the most complete account and has become the gold standard in the literature over the past two decades.25 To explain the varieties of disgust, they enlist a variety of explanations, using Angyal and Freud, as well as Douglas and Darwin.26 In their account disgust has oral origins, arising variously from a distaste of 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. Cultural dietary and food preparation rules serve to separate foods from their animal nature and help us not to think too hard about the process that brought them to our plate. Otherwise we would not be able to consume them.
Rozin and Haidt argue that the fear of oral incorporation of animal products 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. They claim that this is because humans have to deal with the existential terror of knowing that they are animals and, as such, are condemned to die. Disgust develops to repress thoughts of mortality—a Freudian idea where one part of the brain represses another. Hence, certain sexual acts and envelope violations remind us of our animal nature, and poor hygiene places us below the level of humanity. The Rozin and Haidt standard model of disgust also has two further domains: interpersonal disgust, which they say serves to protect the body, the soul, and the social order; and moral disgust.
Outside of science, writers in the humanities have made rich and potent contributions to the literature on disgust. William Ian Miller has a terrific description of what he calls “life soup” in his wonderful book The Anatomy of Disgust: “Temperature, it seems, disgusts precisely in those ranges in which life teems, that is, from the dank of the fen to the mugginess of the jungle; this is the range in which sliminess exists, for slime ceases to be when frozen solid or when burnt to a crisp. The temperature must be sufficient to keep the old life soup bubbling, seething, wriggling and writhing but not so great as to kill it” (64). However, despite Miller’s description being spot-on for the conditions that nurture pathogens, he resists a biological explanation—preferring Freudian interpretation. He concludes that “ultimately the basis for all disgust is us—that we live and die and that the process is a messy one, emitting substances and odours that make us doubt ourselves and fear our neighbours.”
Robert Rawdon Wilson, a Shakespeare scholar, fearlessly explores some of the darkest regions of disgust, both physical and sexual, and asks why it repulses, but at the same time fascinates. He proposes many positive uses for disgust, for example, in humor that ridicules immoral behavior and in marking the boundaries of the acceptable. Yet despite the breadth and depth of his exploration, Rawdon Wilson has to admit defeat. He labels disgust “the hydra” because he finds it too complex to explain.27
While these works are fascinating and illuminating, all of them propose convoluted explanations of disgust, and all give short shrift to biological explanations. An increasing number of scientists—including Daniel Fessler, Debra Lieberman, Josh Tybur, Mark Schaller, Richard Stevenson, and my group—are exploring disgust from a modern evolutionary perspective. For us, there is a simple and parsimonious solution to the puzzle of disgust: disgust systems 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 orchestrates behavior in the direction of pathogen avoidance—whether the pathogens are in the environment, in other animals, or, especially, in other humans. It prevents the entry of pathogens through multiple portals: the skin, the airways, the genitals, as well as the mouth. No magical folk beliefs, Freudian repression, or existential denial of death is needed to explain disgust.
That the human disgust system is a product of evolution does not, of course, mean that it does not vary from individual to individual or from culture to culture. Individuals inherit differing propensities to disgust, and individuals tune their disgust responses over their lifetime according to experience and local cultural rules (especially when it comes to food).28 Nor does it mean that disgust did not take on an important role in moral behavior as humans inexorably evolved into an ultrasocial species. Disgust can appear to be a hydra, utterly confusing in all of its extraordinary and powerful manifestations. But there can surely be little doubt that the disgust system does have a single basic epidemiological function: it evolved to orchestrate the avoidance of pathogens and parasites.
CHAPTER TWO
INTO THE HOT ZONE
May I never lose you, oh, my generous host, oh, my universe. Just as the air you breathe, and the light you enjoy are for you, so you are for me.
Primo Levi, “Man’s Friend”
To make an animal takes proteins, fats, starches, fluids, and micro-nutrients. These ingredients combine to form a tempting calorie-and nutrient-rich dish for other animals to feast on. We are all familiar with the food web: larger, stronger, faster predators eat smaller, weaker predators, which eat smaller, weaker ones, and so on down to the herbivores grazing on the autotrophic plants, bacteria, or algae that fuel the whole system.
But there is more than one way to make a meal of another animal. Rather than investing lots of energy in the hunt and chase, some animals have evolved a less dramatic strategy—parasitism. These animals climb on board, worm their way in, and stow away. They then feast on a smorgasbord of tissues and bodily fluids, not to mention taking advantage of the shelter, transport, and mating opportunities offered by their hapless host.
The parasitic way of life is a pretty good one and explains why parasites outnumber predators on the planet, both in terms of number of species and in total biomass.1 Imagine, for a moment, one of those BBC wildlife series where we see life at night through an infrared lens. The shapes of warm animal bodies show up bright red against their cool nocturnal environment. Pink birds fly through a dark purple sky. Lizards glow yellow or orange. David Attenborough says breathlessly to the camera, “And look at the glowing patch left in the nest as the owl takes off on her nightly hunt!” Now, instead of looking at the world through a heat-detecting lens, switch to a parasite-detecting lens. What does the world look like? In fact, it looks much the same, but in place of the birds and the lizards are silhouettes of parasites. The animal bodies are bright red.
Parasites are everywhere, infe
sting skin, tissues, and guts; even the follicles of your eyelashes teem with microscopic worms. Every free-living animal is a seething mass of parasites. Our parasite-detecting lens reveals not just the fleas, lice, and ticks hiding in the pelt of the animal we are filming; it also shows the worms in its gut, the microbes in its flesh, and the millions of viruses that infest its every cell. Seen through this lens, all animals light up bright red—they are hot zones full of parasites.
Yet most animals do a good job of staying whole, of keeping their delicious bodies to themselves, of staying alive, with their parasites under control, at least for long enough to procreate. No one has yet been able to build a detection system that can scan for tiny bugs and invisibly small microbes hiding inside living organisms. But animals do have systems for detecting and avoiding parasites. And their parasite radar must be trained on particular parasites, those that are particularly risky to those particular animals. Mice need to avoid mouse nematodes, not fish nematodes. Rhinos have to avoid rhino viruses and not human influenza viruses. Every animal has to be able to detect the types of parasite that are specific to its kind. So a well-designed animal should have a parasite-detection system that is capable of detecting not just any parasite hot spot, but those that contain the most threatening varieties of parasite.
But if parasites can’t be seen and they don’t give off any radiation that can be detected on film, what’s an animal to do? For example, if a lobster meets another lobster giving off an odd odor, then maybe it shouldn’t share a den with it, as it might be infected with a lethal virus. Or if a killifish encounters another killifish with black lumps all over its body, then perhaps it should find another shoalmate. If a salamander is hungry, perhaps it shouldn’t risk dining on another salamander of the same species, as it might ingest pathogens infectious to salamanders. And a reindeer should probably migrate regularly so as to avoid eating grass contaminated with parasites’ cysts in the droppings of other reindeer.
All of the animals that are alive today have ancestors that were good at parasite detection and avoidance. Those that didn’t have those abilities simply got eaten up and so ended their genetic history. Animals filter incoming sensory information—sight, touch, taste, and smell—use it to compute likely parasite risk, and then respond to that risk, just as if they really did come equipped with parasite-detecting lenses. This skill seems to be found in all animals, humans included. And we humans have given our parasite-detecting devices a name: “disgust.” Though we may have invested it with special significance and a special name, the human parasite-detection-and-avoidance system doesn’t differ much from that of other animals, and surely it must share common ancestry.2 We humans have a few unusual abilities, built on top of our animal abilities; like our capacity to imagine parasites, and to learn from what we imagine, and our skill in the use of microscopes (real parasite-detecting lenses). But for the most part, we behave as most animals do. So if we want to understand human disgust-related behavior, we should turn to other animals.
Animals have four ways to avoid paying the dire fitness costs of being invaded by body snatchers. First, they can avoid close contact with animals of their own species, especially when they are sick, because this is where the best-adapted and most infectious parasites are likely to lurk. Second, they can avoid other species of animal that might vector parasites that can jump from species to species. Third, they should stay away from places and things that might be contaminated with parasites or their progeny. And finally, particularly enterprising animals can alter the world they live in, in such a way as to make it inhospitable to parasites.3
Task 1: Avoid Others, Especially if They Are Sick
While there are various reasons why animals of the same species might cuddle up to one another, intimacy is far from a great idea when viewed through parasite-detecting lenses. Female house mice (Mus musculus), for example, take a good sniff of prospective mates, and if they detect a whiff of the protozoan worm-like parasite Eimeria vermiformis, they move on to the next male.4 In one famous experiment, researchers painted red lumps on the wattles of the males of half of a flock of sage grouse (Centrocercus urophasianus) to mimic the effect of an ectoparasite infestation. These apparently lousy males had far less mating success than those that had not been so adorned.5
Choosing a healthy-looking bird as a mate has two advantages: it helps get good genes into your offspring, and it prevents you from catching something nasty, like a louse carrying a virus, in the here and now. An unhealthy partner could make you sterile or, worse yet, could introduce congenital disease into your breeding line. Disease avoidance therefore offers a good additional evolutionary explanation for why birds prefer healthy-looking birds as mates.6
Another way that animals test the health of a prospective mate is to provoke them to fight each other and see who comes out on top. Female squirrels and possums display their sexual availability prior to estrus, which leads to competition between males. The winner of the battle, which is likely to be the healthiest and least parasite-ridden, gets the girl.7 Humans may be missing a penis bone for similar reasons. Having a big showy erection is a great way of displaying to a prospective mate that you don’t have any fulminating diseases that could interfere with all those delicate hydraulics.8
In general it’s advantageous to stay away from sick individuals of the same species. About 7 percent of bullfrog (Rana catesbeiana) tadpoles have a yeast infection that reduces their mobility and may lead to death. Given the choice, healthy tadpoles avoid going anywhere near those that have the infection.9 Similarly, when experimenters injected killifish (Fundulus diaphanus) with black ink spots to mimic the effects of a common parasite, other killifish preferred not to shoal with them.10 Caribbean spiny lobsters (Panulirus argus), usually social creatures, refuse to share dens with lobsters infected with the PaV1 virus.11
Parasite-detecting lenses are particularly helpful if you are a social species. While being social has its advantages—such as safety in numbers and the benefits of cooperation—it has a big downside in the form of greater risk of disease. Social primates are careful who they accept into the troupe; they will generally welcome a new member only after a long period of quarantine. During that time the troupe will often attack the outsider, testing its state of health. Any overt signs of sickness decrease the chances of acceptance.
Parasite pressure may actually place a limit on group size—in habitats rich in pathogens, such as the warm, humid rain forest, typical troupe size for colobus monkeys is about nine, while in the hot dry savannah of highland Ethiopia, with much lower pathogen loads, gelada (Theropithecus gelada) group size can run to several hundred.12 Through parasite-detecting lenses, members of foreign troupes appear as parasite hot zones—especially because they might be carrying new pathogen variants, ones that the home group have no immunity to. Parasite pressure may be why primates are careful to limit contact with foreign groups, communicating only at a distance by calling, and by giving way to each other when they cross in the forest. Instinctive xenophobia may be a useful adaptation for a social species.
Another good way of not catching a parasite is to avoid meat, especially that from one’s own species. Ecologists have puzzled over why cannibalism is so rare, observing that very few species satisfy their nutritional needs by nibbling on their neighbors. Parasites offer an explanation: one’s cousin is a hot zone. A relative is more likely to carry an infection infectious to oneself than is a more distant species. The larvae of tiger salamanders (Ambystoma tigrinum), for example, have cannibal and noncannibal varieties, but the cannibals tend to carry much higher numbers of intestinal nematodes and bacteria than their noncannibal cousins.13
Humans, also, are adept at avoiding catching diseases from others of the same species. We sit as far as possible away from others at table or on trains; if someone shows any visible signs of disease, we tend to avoid contact and terminate interaction early;14 and we turn cannibal only in extreme circumstances. Indeed, three of the six categories of human
disgust response that our study identified concern others of the same species—people who look sick, abnormal, or disfigured; people as sex partners; and people who display poor hygiene.15
Task 2: Stay Away from Other Species, Especially Parasites, Parasite Hosts, and Vectors
Apart from their own kind, what further parasite hot spots might well-adapted animals avoid? Other animals that are also parasites themselves, that host pathogens, and that are used by pathogens as vectors all pose threats. Animals have evolved amazing repertoires of behaviors to defend against such risks.
Take Caenorhabditis elegans, for example. This tiny nematode worm, with only 302 neurons to its name, is much beloved by biologists as a model system for understanding animal physiology and behavior. This 1-mm-long creature is clever enough to detect a parasitic bacterium in its petri dish and turn around and flee from it, in seconds (see the film on the book website). When it is offered to nonparasitic bacteria to eat, however, it worms quickly over to gobble it up.16 Ants are similarly discriminating, feeding on the corpses of other species, but scorning those infested with parasites.17 Fish are known to avoid disease vectors; the rainbow trout (Oncorhynchus mykiss) can detect and swim away from parasitic eye flukes that cause blindness and, as a result, suffer fewer infections.18
The surface of an animal is like a tablecloth spread for a picnic, inviting hordes of hungry parasites to a free meal. Multiple species of lice, fleas, ticks, mites, bloodsucking flies, mosquitoes, leeches, bacteria, and fungi exploit or colonize the epidermis of every species of vertebrate. And vertebrates invest a lot of effort to get rid of them. Cattle stamp their feet and swing their heads in response to biting tsetse flies; fish scrape themselves on rocks and vegetation, as do elephants. Vampire bats (Desmodus rotundus) scratch to remove bat flies,19 while birds preen, and impala (Aepyceros melampus) use their teeth as tick combs. When an experimenter stopped up the gaps in an impala’s teeth on one side only, the side of the body that thus couldn’t be groomed rapidly became tick-infested.20
Don't Look, Don't Touch, Don't Eat: The Science Behind Revulsion Page 3