The 10,000-year bender: Why humans love a tipple

(image: Tom Gauld)

Our taste for alcohol results from an evolutionary tussle between humans and yeast – one in which the microbes have often had the upper hand

EVEN if you are teetotal, you cannot deny that humans, as a species, like to drink. We consume wine, beer, cider, spirits... in fact, the fermented product of almost anything we can turn to alcohol. Our fondness for this toxic substance, the cause of so much trouble, is something of a mystery. Maybe it is enough to say that we drink because it makes us feel good. But I think that to understand our love of alcohol you need a bigger, more evolutionary, explanation.

The story of alcohol is one of an intimate relationship between humans and yeasts, an affair that began millions of years ago and is still playing out today. We like to cast ourselves as the star of this drama, but in fact yeasts are the unsung lead character. Ours is a symbiotic connection - a mutually beneficial partnership. It is also one in which the balance of power is constantly shifting. If anything, the yeasts seems to have had the upper hand, at least since our ancestors began brewing their own grog. We cultivate yeasts, ensuring they survive and thrive, and in return we get, at best, a good night out and a hangover the next morning. Once upon a time, however, yeast and alcohol may have offered us more significant rewards.

Today the costs of our love of alcohol often outweigh any benefits. But, being a story of evolution, it doesn't end there. Already some humans have acquired genetic changes that encourage them to drink less. If this trend continues, it is possible that one day this long and tempestuous relationship will reach a kind of tenuous truce.

We are not the only species that likes a tipple. Fruit flies regularly consume fermented fruit, seemingly without any impairment to their faculties. Other animals don't hold their drink so well. Cedar waxwings have been spotted partaking of a few too many overripe winterberries and then flopping around among the branches of trees or crashing into buildings. Terrifying accounts of drunk elephants exist, although these are poorly substantiated. There are even records of creatures going out of their way to become intoxicated. These include tree shrews - the closest living relatives to the primates - which seek out nightly nips of a frothy "wine" produced by yeast in the flower buds of the bertam palm.

This kind of behaviour can be traced right back to the evolution of fruit around 130 million years ago, when flowering plants emerged during the Cretaceous era. With a new source of food available, a genus of yeasts known asSaccharomyces evolved to feed on it, and in the process these yeasts acquired a new physiological trick. Instead of using their energy to break down sugar completely, they evolved the ability to partially break it down, producing ethanol as waste when sugar supplies were abundant and oxygen scarce. The partial breakdown of valuable sugars meant that these yeasts were actually less efficient than their forebears. But it gave them a big advantage too. Ethanol kills most bacteria, and bacteria like to feed on fruit, so producing alcohol allowed yeasts to kill off the competition.

From the beginning, Saccharomyces would have fed on ripe fruits - unripe ones often being toxic - so the smell of ethanol might have become a universal sign that fruits were ready to eat. According to Robert Dudley at the University of California, Berkeley, natural selection favoured primates and other fruit-eating mammals that could use the odour of ethanol to locate edible fruit in vast forests. He believes they evolved a fondness for the smell that led them to experience positive sensations even before they consumed the alcohol itself (The Quarterly Review of Biology, vol 75, p 3). According to this theory, every time a primate sniffs booze, pleasure rings out in its brain. Incidentally, we primates may not be alone in this. Fruit flies' mouths have a sensory receptor, a kind of taste bud for alcohol. It was identified by a grad student who, in a moment of frustration, offered them beer.

Love at first sight?

Dudley suggests that our ancestors began to make alcohol to feed their sensory bias for it, in much the same way that we farm sugar cane and sugar beets to feed our evolved preference for sugar. If so, alcohol is like all the other things from which we once benefited but now overindulge in. Not everyone is convinced. Doug Levey of the National Science Foundation in Arlington, Virginia, believes primates never had an innate tendency to seek out the smell of ethanol - after all, fruit that smells of ethanol is already en route to being overripe. Instead, he argues, our ancestors only really started enjoying alcohol after they learned to make it themselves. By neurological happenstance, the liquor triggered feelings that they liked and desired more of, and so they sometimes indulged to excess (Integrative & Comparative Biology, vol 44, p 284). If Levey is right, our taste for alcohol is more like our taste for caffeine or cocaine than for sugar.

Alcohol does produce pleasurable feelings - this much no one debates - through its ability to bind to GABA receptors in the brain. Normally, these receptors reduce the activity of the neurons on which they are found, but when alcohol binds to them it releases that pent-up activity and, in doing so, relaxes both our bodies and our inhibitions. Thanks to this, countless babies have been conceived, countless friendships formed and rapprochements achieved. But ethanol also makes us uncoordinated, groggy, reckless and aggressive. It is the fuel behind many accidents, fights and even wars.

Overall, then, alcohol consumption may not have been advantageous to our ancient fruit-gathering ancestors but, interestingly, it seems to have offered real benefits once we began to farm. At the dawn of agriculture, around 10,000 years ago, people in small settlements began to ferment foods and drinks. This would have allowed them to preserve surplus grain, in essence by favouring yeasts in place of food-spoiling bacteria. It would even have made grain more nourishing because yeasts produce other nutrients, including B vitamins, during fermentation. Alcohol consumption might also have helped smooth social interactions, which would have become more complex as communities grew. Perhaps most importantly, fermentation offered a way to sterilise liquids, since ethanol kills not only bacteria - including the one that causes cholera - but also other pathogens. Indeed, animals may self-medicate with it. For example, fruit flies infested with parasitic wasps consume more alcohol, which usually kills the wasp without being fatal to the flies. In the unsanitary conditions faced by early settled communities, fermented drinks were both nutritious and potable - not entirely healthy, but better than unfermented alternatives.

As for how we learned to make alcohol, most anthropologists believe that the first farmers stumbled across the trick by accident, when stored wheat and barley became contaminated with Saccharomyces yeasts. There is another, more intriguing, possibility. Anthropologist Solomon Katz at the University of Pennsylvania in Philadelphia has argued that fermentation came first, giving our ancestors a strong incentive to cultivate grain to make grog. As it happens, the oldest vessel for storing alcohol found so far, 7000 years old, is contemporaneous with or may even predate the earliest evidence of farming in China, where it was unearthed (PNAS, vol 101, p 17593).

Either way, once alcohol had been manufactured, its producers realised that it could be made again and again simply by taking a sample from one fermenting liquid and using it to kick-start the process in a new batch. It must have seemed like a magical transformation to ancient brewers, but today we know that humanity's first vats were colonised by Saccharomyces cerevisae. We also have its precise genetic code: it was one of the first organisms to have its genome sequenced. However, we still know very little about basic matters such as where it came from.

An evolving partnership

Brewer's yeast has changed many times as agriculture spread and different human cultures emerged (Comptes Rendus Biologies, vol 334, p 229). New forms, as distinctive as species, emerged in association with beer and wine production in different regions. Some of these yeasts changed further to give a wide variety of bread yeasts. In a monk's cave in Germany, the cold-tolerant yeast used to make lager evolved as a hybrid of S. cerevisae and a species that hails from Patagonia. Mysteriously, this occurred more than 100 years before Europeans reached the New World (PNAS, vol 108, p 14539).

In Britain and elsewhere, brewers also began to use an entirely different genus of yeasts, Brettanomyces, which had acquired the ability to produce alcohol independently of Saccharomyces, from which it split 200 million years ago. Brettanomyces is used in the production of several speciality beers, giving an unusual sour, tangy flavour.

Humans have undoubtedly influenced the evolutionary diversification of yeasts, but we did not consciously steer the process any more than the Galapagos Islands controlled the evolution of Darwin's finches. Fungi such as yeasts often interact symbiotically with other species. Leaf-cutter ants, for example, feed bits of leaf to the fungi in their nests, which in turn produce fruiting bodies that the baby ants eat. Ambrosia beetles carry fungi in little pouches, releasing them onto dead wood where they grow, providing food for their larvae. In these and other cases, animals are often said to have domesticated fungi, but perhaps the reverse is true. After all, the animals are forced to forage and ferry while the fungi just feed, grow and reproduce. Likewise, brewers have to work hard to ensure that their yeasts thrive. What's more, those varieties that take the most advantage of us are most likely to survive. These include lineages that have evolved to tolerate higher concentrations of alcohol, allowing them to produce more potent brews, so persuading us to work even harder to cultivate them.

The yeasts have shaped us directly, too. One key change occurred very early - a big divergence between humans and other primates in levels of the enzyme that breaks down alcohol, and where in the body it is found. In non-human primates, alcohol dehydrogenase is found throughout the body. That seems unsurprising as ethanol is a by-product of various bodily processes, so most cells encounter it. The enzyme is also everywhere in our bodies, but it is disproportionately concentrated in the liver, where the alcohol we imbibe ends up. Our ancestors' increasing consumption of alcohol became increasingly dangerous: a blood alcohol level of 0.4 per cent is considered lethal for adult humans. Those who survived binges tended to have more alcohol dehydrogenase in their liver because they could process alcohol more rapidly. Today, 10 per cent of the enzymes in the average human liver are dedicated to metabolising ethanol.

Given the longstanding relationship between humans and brewer's yeasts, it is not surprising that each has influenced the other's evolution. This process is ongoing. No symbiotic relationship is simple - the costs and benefits that each party experiences shift with time and context. Alcohol may once have been a signal of good fruit; in the early days of agriculture, it probably aided our survival. But the balance would have tipped as waterborne diseases became less of a problem and as yeasts became easier to cultivate and their products more intoxicating. People may still benefit from the occasional drink: every few years a study comes out arguing that a little bit of wine or, more rarely, beer is good for you. However, for society as a whole, alcohol now brings more costs than gains, whether measured in life expectancy or money. In 2010, alcohol was the third biggest health risk globally, killing 4.9 million people worldwide (The Lancet, vol 380, p 2071), and problem drinking has an annual economic burden of hundreds of billions of dollars.

In some places, such costs seem to have been incurred for many generations, long enough to allow people to evolve once again. This time, natural selection has favoured an adaptation that encourages individuals to consume less alcohol. The detoxification of ethanol involves two enzymes - alcohol dehydrogenase, to turn ethanol into acetaldehyde, and aldehyde dehydrogenase, which converts acetaldehyde to acetate. This enzyme partnership exists in nearly every organism, including many bacteria, but in some East Asian populations, including most Chinese and Japanese people, the gene for aldehyde dehydrogenase is broken. When people with this version of the gene consume alcohol, drunkenness occurs after fewer drinks, their faces turn red, their hearts palpitate and they feel nauseous.

The mutated gene spread in geographic and temporal lockstep with the spread of rice cultivation and rice wine production some 7000 to 10,000 years ago (BMC Evolutionary Biology, vol 10, p 15). Researchers say it may have evolved for a reason, pointing out that once it arose, it spread more quickly than it would have by chance. They argue that East Asian populations had started to feel the negative consequences of alcohol so strongly that individuals whose bodies discouraged them from drinking to excess were more likely to survive. In this light, the "drink less" gene variant might have been favoured both by natural and sexual selection, at least if ruddy-faced drunks are less likely to find mates.

Evolution does not stand still, so it is interesting to speculate that various "drink less" mutations may be spreading in human populations right now. If so, then one day our love affair with alcohol might end - though one should not underestimate the evolutionary cleverness of yeasts.

In the meantime, alcohol-producing yeasts will keep evolving, as will our understanding of humanity's intimate relationship with them. Despite the story I have told, more remains unresolved than resolved, hidden in every alcoholic drink. So, while we can still enjoy it, let's raise a glass to the yeasts. Curse them, and bless them!

Rob Dunn