Cheerful Chimps: Are Animals Really Happy When They Smile?

A smiling face might not signal what we think, if there’s anything to be learned from other primates.

By Frans de Waal|Friday, May 31, 2019
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Alison Mackey/Discover using photos from Avalon/Photoshot License/Alamy Stock Photo

I can’t stand TV sitcoms and Hollywood movies featuring monkeys and apes. Every time I see a dressed-up simian actor produce one of their silly grins, I cringe. People may think they’re hilarious, but I know their mood is the opposite of happy. It’s hard to get these animals to bare their teeth without scaring them — only punishment and domination can call forth these expressions. Behind the scenes, a trainer is waving his electric cattle prod or leather whip to make clear what will happen if the animals fail to obey. They are terrified.

The bared-teeth grin is not to be confused with a wide-open mouth and intense staring eyes. That fierce face, which looks like an intention to bite, acts as a threat. In a grin, the mouth is closed, but the lips are retracted to expose the teeth and gums. The row of bright white teeth makes it a conspicuous signal, visible from far away, yet its meaning is the exact opposite of a threat.

Many questions surround the grin, such as how this toothy expression became a friendly one in our species and where it came from. The latter question may seem odd, but everything in nature is a modification of something older. Our hands came from the forelimbs of land vertebrates, which derived from the pectoral fins of fish. Our lungs evolved out of fish bladders.

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Alison Mackey/Discover, using photo from Master305/Shutterstock

A Social Signal 
The grin, it seems, derives from a defensive reflex. For example, when we peel a citrus fruit — an action that risks spraying drops of acidic juice into our face — we automatically pull our lips back from our teeth. I’ve observed baboons grinning to avoid perforating their lips while eating a succulent cactus.

Fear and unease also pull at the corners of our mouths. Films of people riding roller coasters often show not delighted smiles but terrified grimaces. The same happens in other primates. In a rhesus monkey group at the Vilas Park Zoo in Madison, Wisconsin — where I studied as a primatologist — the mighty alpha female, Orange, needed only to walk around to evoke the expression from others in her troop. All the females she passed would flash her grins — especially if she walked in their direction, and even more so if she honored their huddle by joining them. None of them moved out of her way, but the expression told her, “I’m subordinate, I’d never dare challenge you.” Orange was so secure in her position that she rarely needed to use force, and by showing their teeth, the other females removed any reason she might have had for throwing her weight around.

Among rhesus monkeys like Orange and her troop, this expression is 100 percent unidirectional: It is given by the subordinate to the dominant, never the other way around. As such, it is an unambiguous marker of the hierarchy. Every species has signals for this purpose, though. Humans signal subordination by bowing, groveling, laughing at the boss’s jokes, kissing the don’s ring, saluting and so on. Chimpanzees lower themselves in the presence of high-ranking individuals and issue a special kind of grunt to greet them. But the original primate signal to make clear that you rank below someone else is a grin with the mouth corners pulled back.

However, far more underlies this expression than fear. When a monkey is simply scared, such as when it spots a snake or predator, it freezes to avoid detection or else it runs away as fast as possible. This is what plain fear looks like.

The grin, though, is an intensely social signal that mixes fear with a desire for acceptance. It is a bit like the way a dog may greet you, with flattened ears and tucked-in tail, while rolling on his back and whining. He exposes his belly and throat while trusting that you will not use weaponry on his most vulnerable body parts. No one would mistake the canine rollover for an act of fear because dogs often behave this way while approaching the other as an opening move. It can be positively friendly. The same applies to the monkey grin: It expresses a desire for good relations. Hence, Orange received the signal many times a day, whereas a snake never would.

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Alison Mackey/Discover, photo by Bronwyn Photo/Shutterstock

From Grins to Smiles 
The great apes go a step further: Their grin, although still a nervous signal, is more positive. In many ways, their expressions and the way they use them are more like ours. Bonobos, who often mate face to face, sometimes bare their teeth in friendly and pleasurable situations, such as during sexual intercourse. One German investigator spoke of an Orgasmusgesicht (orgasm face) given by females while they stare into their partner’s face. They may also use the same expression to calm down or win over others and not purely along one-sided hierarchical lines, as in the monkeys.

Dominant individuals also bare their teeth when they try to reassure others. For example, when an infant wanted to steal a female’s food, she dealt with it by gently moving the food out of his reach while flashing a big grin from ear to ear. This way she prevented a tantrum. Friendly grins are also a way to smooth things over when play gets too rough. Only rarely do apes lift up their mouth corners during a grin, but if they do, it looks exactly like a human smile.

Sometimes, though, a grin isn’t welcome. Male chimpanzees — who are always in the business of trying to intimidate one another — don’t like to reveal anxieties in the presence of a rival; it’s a sign of weakness. When one male hoots and puts up his hair while picking up a big rock, it may cause unease in another because it announces a confrontation. A nervous grin may appear on the target’s face.

Under these circumstances, I have seen the grinning male abruptly turn away so that the first male can’t see his expression. I have also seen males hide their grin behind a hand, or even actively wipe it off their face. One male used his fingers to push his own lips back into place, over his teeth, before turning around to confront his challenger. To me, this suggests that chimpanzees are aware of how their signals come across. It also shows they have better control over their hands than over their faces.

The same is true for us. Even though we can produce expressions on command, it’s hard to change one that comes up involuntarily. To look happy when you are angry, for example, or to look angry when in reality you are amused (as may happen to parents with their children), is nearly impossible.

The human smile derives from the nervous grin found in other primates. We employ it when there is a potential for conflict, something we are always worried about even under the friendliest circumstances: We bring flowers or a bottle of wine when we are invading other people’s home territory, and we greet each other by waving an open hand, a gesture thought to originate from showing that we carry no weapons. But the smile remains our main tool to improve the mood. Copying another’s smile makes everyone happier, or as Louis Armstrong sang: “When you’re smiling, the whole world smiles with you.”

Reprimanded children sometimes can’t stop smiling, which risks being mistaken for disrespect. All they’re doing, though, is nervously signaling non-hostility.

I seriously doubt that the smile is our species’s “happy” face, as is often stated in books about human emotions. Its background is much richer, with meanings other than cheeriness. Depending on the circumstances, the smile can convey nervousness, a need to please, reassurance to anxious others, a welcoming attitude, submission, amusement, attraction and so on. Are all these feelings captured by calling them “happy”?

Our labels grossly simplify emotional displays, like the way we give each emoticon a single meaning. Many of us now use smiley or frowny faces to punctuate text messages, which suggests that language by itself is not as effective as advertised. We feel the need to add nonverbal cues to prevent a peace offering from being mistaken for an act of revenge, or a joke from being taken as an insult. Emoticons and words are poor substitutes for the body itself, though: Through gaze direction, expressions, tone of voice, posture, pupil dilation and gestures, the body is much better than language at communicating a wide range of meanings.

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Alison Mackey/Discover based on Cameris/Shutterstock; Koldunova Anna/Shutterstock

One and the Same 
There is an old claim, repeated over and over in the scientific literature, that we have hundreds of muscles in our faces, far more than any other species. But there is really no good reason why this should be so. When a team of behavioral scientists and anthropologists finally tested the idea by carefully dissecting the faces of two dead chimpanzees, they found the exact same number of muscles as in the human face — and surprisingly few differences.

We could have predicted this, of course, because Nikolaas Tulp, the Dutch anatomist immortalized in Rembrandt’s painting The Anatomy Lesson, had reached a similar conclusion long ago. In 1641, Tulp was the first to dissect an ape cadaver and said that it was the spitting image of the human body in its structural details, musculature and organs.

Despite these similarities, the human smile differs from the ape equivalent in that we typically pull up our mouth corners and infuse the expression with even more friendliness and affection. This applies only to the real smile, though. We often wear plastic smiles with no deep meaning whatsoever. The smiles of airplane personnel and smiles produced for cameras (“say cheese!”) are artificial, for public consumption.

Only the so-called Duchenne smile is a sincere expression of joy and positive feeling. In the 19th century, the French neurologist Duchenne de Boulogne tested facial displays by electrically stimulating the face of a man who lacked pain perception. Duchenne produced and photographed all sorts of expressions this way, but the man’s smiles never looked happy. In fact, they looked fake.

One time, Duchenne told the same man a funny joke and triggered a much better smile because instead of just smiling with his mouth, as he had been doing thus far, he now narrowed the muscles around his eyes as well. Duchenne perceptively concluded that while the mouth can produce a smile on command, the muscles near the eyes don’t obey as well. Their contraction completes a smile to indicate genuine enjoyment.

A Window Into Our Emotions 
That our faces most of the time mirror true feelings may seem obvious enough, but even this simple idea was once controversial. Scientists strenuously objected to Charles Darwin’s use of the term expression as too suggestive, as implying that the face conveys what’s going on inside. Even though psychology literally is the study of the psyche — Greek for “soul” or “spirit” — many psychologists didn’t like references to hidden processes and declared the soul off limits. They preferred to stick to observable behavior and regarded facial displays as little flags we wave to alert those around us to our future behavior.

Darwin won this battle too, because if our facial expressions were mere flags, we should have no trouble choosing which ones to wave and which to leave folded. Every facial configuration would be as easy to summon as a fake smile. But in fact, we have far less control over our faces than over the rest of our bodies. Like chimpanzees, we sometimes hide a smile behind a hand (or a book, or a newspaper) because we’re simply unable to suppress it. And we regularly smile, or shed tears, or pull a disgusted face while we are unseen by others, such as when we are talking on the phone or reading a novel. From a communication perspective, this doesn’t make any sense. We should have completely blank faces while talking on the phone.

Unless, of course, we evolved to communicate inner states involuntarily. In that case, expression and communication are the same thing. We don’t fully control our faces because we don’t fully control our emotions. That this allows others to read our feelings is a bonus. Indeed, the tight link between what goes on inside and what we reveal on the outside may well be the whole reason why facial expressions evolved.

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