Tracing the intricate interactions between yeasts, apes, and early human ancestors, Rob Dunn reveals how yeasts have shaped our biology, diets, and even societal structures.
Humans engage in mutualisms (mutually beneficial relationships) with many species; scientists describe a subset of these relationships as domestication, where one species exerts control over the other. For example, we might say that leaf-cutter ants have domesticated the fungi that they grow to feed their babies, or that some ants have domesticated the aphids that they rely on as cattle, ferrying them from branch to branch and protecting them from predators and parasites. Generally, when a mutualism involves an animal and a plant or an animal and a fungus, we describe the animal as domesticating the plant or fungus. But often this distinction is unclear; one could easily argue, for example, that fungi have domesticated leaf-cutter ants as demonstrated by the extent to which they have altered the behaviour, diet, reproduction and even the shape and size of the ants. One could also argue, as I do here, that yeasts have domesticated humans.
For tens of millions of years, the ecology of yeasts was a story of the relationship between plants, sugar and insects. Yeasts are single-celled fungi that tend to live sweet, sugar-dependent lives. They eat sugar and, in doing so, produce carbon dioxide and/or alcohol as waste. The challenge for yeasts has long been that, lacking legs, wings or even flagella, they are relatively unable to reach the sugar they need in sap or nectar. Yeasts deal with this problem by catching rides from sugar-loving insects such as wasps or fruit flies. The yeasts produce aromas specifically tuned to the smell receptors of insects (Christiaens et al. 2014). The insects follow their “noses,” as it were, to the good smells, find nectar and, also, unwittingly carry the yeasts from here to there and back again (Madden et al. 2018). The guts of social insects, such as wasps, have also been shown to be safe places for yeasts to overwinter, protected from the elements (Stefanini et al. 2016). In some cases, the insects also benefit from these relationships in that they can use the aromas produced by yeasts – e.g., the smells of beer, wine or bread – to find sugar sources. Yeasts and insects, then, are in relationships in which the yeasts benefit from the insects and the insects sometimes benefit from the yeasts. The relationship, however, is neither so intimate nor so specialized that one might describe it as domestication. Then apes evolved.
The relationship was sufficiently transformative so as to alter the genomes of every ape to have lived since, including every human.
We now know that at some point around ten million years ago – about the time of the common ancestor of orangutans, gorillas, chimpanzees and humans – apes entered into a new relationship with yeasts. The relationship was sufficiently transformative so as to alter the genomes of every ape to have lived since, including every human. It is thought that apes first encountered yeasts in rotten fruits. When fruits rot, they can become covered in filamentous fungi (AKA, mold), which is often unsafe to ingest. They can become colonized by lactic acid bacteria – like those found in yogurt – in which case they become acidic and safe to eat (think sauerkraut). Or they can become colonized by yeasts and become alcoholic. In practice, many tropical fruits are probably a mixture of lactic and alcoholic, like sour beer.
The drunken monkey hypothesis suggests that as apes spent more time on the forest floor (having become too big to move as readily among the trees as had their ancestors) that they began to eat more rotten fruit (Dudley 2014). The evolutionary evidence for this change is threefold. Roughly ten million years ago, apes evolved a version of the alcohol dehydrogenase gene capable of metabolizing alcohol forty times faster than the previous version. The version of the gene allowed apes to get many more calories from alcohol than they might otherwise; this change, along with others we don’t yet fully understand, may have also made them more likely to get buzzed and hence to feel rewarded for their choice (Carrigan et al. 2015). In addition, recent research by Claudia Staubert and colleagues has shown that at about the same time (give or take a few million years) apes also evolved new receptors for lactic acid, like that found in fermented fruits. Those receptors, when stimulated, trigger ape bodies to stop burning fat and also send signals to the immune system to calm down. Both responses would benefit apes that were eating rotten fruit in that they would tell the body “stop burning fat, we’ve got sugar,” and “woah, the bacteria in this food aren’t dangerous (Peters et al. 2019).” Finally, recent research on which I collaborated has shown that at some point apes also evolved a preference for sour foods (Frank et al. 2022). Here are hints of an interesting possibility, namely that yeasts and lactic acid bacteria were beginning to domesticate apes. They were starting to trigger changes in ape biology that would make the apes more likely to ingest fermented foods and thus carry the yeasts to new places, including new fruits. In short, they were triggering changes in ape biology that made the apes more like wasps.
In all of these cases, we might describe this as human ancestors fumbling with the domestication of yeasts and bacteria. But we can just as readily describe it as yeasts and bacteria fumbling with the next stages of domesticating humans.
Then, in the story of yeasts and our kind, there is a nine million year gap. It is thought that during this time our ancestors continued to tangle with yeasts. But yeasts don’t turn up readily in the fossil record and so we have few real clues as to the details of these entanglements. What we do know from research by Katie Amato at Northwestern University is that non-human primates show evidence of attempts to control fermentation. For example, some capuchin monkeys appear to knock fruits down to the ground only to come back to them weeks later, once they have become like a kind of wild kombucha (Amato et al. 2021). Such attempts at intentional fruit fermentation are likely to have occurred among our ancestors too; and it wasn’t just fermentations of fruits. John Speth at the University of Michigan has argued that the fermentation of meat by our ancestors is also likely to have been common during this period, even in the tropics (Speth, Morin, 2022). Dan Fisher, also at the University of Michigan, has suggested that Clovis Mammoth hunters in North America used to ferment their mega-leftovers in ponds. A recent study in what is now the Czech Republic found that mammoths showed evidence of being stored on the ground just outside of living sites (the author finds evidence that these piles of fermenting meat were used to attract and feed ravens and then some of those same ravens were being eaten; Baumann et al. 2023). In all of these cases, we might describe this as human ancestors fumbling with the domestication of yeasts and bacteria. But we can just as readily describe it as yeasts and bacteria fumbling with the next stages of domesticating humans.
We live in the yeastocene, an epoch in which single-celled fungi exert startling and disproportionate influence.
The story of yeasts and our ancestors picks up again at the foot of the Zagros mountains in Mesopotamia. Humans began to settle in one place for longer periods of time. This may have been the yeast’s doing. Once humans settled, it was easier for them to take better care of the yeast. And they did; around thirteen thousand years ago humans were gathering grains to feed to beer-making yeasts. What was more, the humans prepared the grains for the yeast, as if in offering. They wet and sprouted the grains so as to begin to convert the starch in the grain to sugars. This conversion, called malting, made the sugars available to the yeasts (Liu et al. 2018). The yeasts were making these settled humans do a lot of work. In order to convince the humans to keep doing this work, some of the yeasts are hypothesized to have evolved to tolerate and produce more alcohol. When and if they did, the humans would have been even more likely to search out more grain or other foods for the yeast.
Eventually, humans began to collect so much grain that they ran short. The fields were bare. And so humans found ways to innovate. They gathered grain from farther away. Then, eventually, they figured out how to plant grains. Doing so gave the farmers the ability to feed far more yeast. This is often described as a moment of great mutualism, between farmers, grains and yeasts. Judged by the metrics evolutionary biologists use, it was. The humans who farmed grains had more food and were able to have more children and to raise more of those children into adulthood. Their evolutionary fitness, which is largely a measure of how many children individuals have, increased (Kovaka et al. 2016). The grains that were chosen also benefited. But the yeasts benefited the most; it is likely that in the first farming villages the total number of individual yeasts outnumbered the total number of humans ever to have lived. But there was something else too: the issue of well-being.
Often, when we humans have domesticated species we have increased their numbers and, hence, their evolutionary fitness. But we have simultaneously decreased their well-being. Compare a wild jungle fowl, the wild relative of domestic chickens, to a domestic chicken that, if given as much food as it can eat, will grow in a little more than a month to a size too big to stand on its own legs. Consider thousands of such chickens, wing to wing and butt to butt. I’m not sure what a chicken values in terms of its well-being, but I think I’d rather be a jungle fowl. The stories of pigs, sheep, and cows are similar. Now, let’s return to the relationship between yeasts and humans. The environments in which yeasts live have always been simple. They’ve always lived cheek to jowl; it isn’t clear that the well-being of a yeast cell in a barrel of beer is different from the well-being of a yeast cell in the intestines of a wasp. Meanwhile, the well-being that declined dramatically once humans began to associate with yeasts is that of humans.
The story of humans, grains and yeasts repeated with variations on the theme in Mesopotamia, China and MesoAmerica. In each case, research by anthropologists now shows that the lives of many, and in some cases most, humans became worse. The social structure of human societies increased as did inequalities. These inequalities made us even more like social wasps or ants. While worker ants live hard lives, the length of which is typically numbered in the weeks, queen ants can live as long as twenty nine years (e.g., Lucas and Keller, 2014). The situation in early settlements was similar, if not quite so extreme, when comparing the lives of human workers and human royalty. Also, new pathogens evolved and old pathogens became more common. Think malaria. Think deadly intestinal parasites. Think, eventually, tuberculosis. Early human settlements were places where humans lived lives of great evolutionary fitness (populations boomed), but where the average individual life was short, brutal and plagued with fevers, boils, diarrhoea, coughing and, more generally, suffering (Cohen and Armelagos, 1984). Here then is a conundrum. In feeding yeasts, humans benefited yeasts but their own well-being declined. This isn’t a conundrum if we think of the story from the other way around; it isn’t a conundrum if we think of yeasts as having domesticated humans.
Through time, the domestication of humans by yeasts and their grains would become more complete in some places. Humans evolved so as to cope with their new starchy diets. They evolved extra copies of amylase genes and, as a result, produced more amylase in their mouths (Perry et al. 2007). This made the humans more likely to perceive grains and other starches as sweet; more likely too to tolerate the humble flavours available in their domesticated diets. In this way, humans were just like dogs or rats, both of which showed similar evolutionary changes in their amylase genes when they were domesticated (Pajic et al 2019). Then there was something else.
For tens of millions of years, yeasts rode from place to place on wasps. But wasps can only fly so far and almost never traverse from one continent to another. By domesticating humans, yeasts also found a way to get from one place to another. They rode us. In part, they rode us by catching rides in or on our containers and implements from place to place. They can ride on spoons or in pots. They rode on barrels in Columbus’s ships. But yeasts also found ways to colonise our very bodies. In a study we undertook a number of years ago with the Puratos Center for Bread Flavor, my colleagues and I were able to show that the hands of bakers (and presumably the rest of their bodies) are covered with yeasts and lactic acid bacteria (Reese et al. 2020). The artist Jiwon Woo has argued that similar things are happening with kimchi and has gone so far as to suggest that the Korean word son mat, for hand flavour, connotes the ancient influence of hands and their microbes on the ecology of kimchi and other fermented Korean foods. These bakers and kimchi makers are vessels for the yeasts. So too, likely, were the bodies of many ancient humans.
Recently, a number of high profile papers have demonstrated negative effects of drinking on well-being, including effects on brain atrophy and cancer (e.g., Rumgay et al. 2021 or Daviet et al. 2022). We love these foods and drinks and feel as though they provide us with benefits, and yet we also suffer their consequences, particularly late in life (notably after their effects on Darwinian fitness are less relevant). But, again, this is only a conundrum if we assume ourselves to have domesticated yeasts. If we think that the yeasts domesticated us, then it is less surprising that the agricultural systems they have made for themselves, the cities they have made for themselves and the human behaviours that they have engineered for themselves – prost – don’t always keep us well. It would be like asking if our modern agricultural system benefits the life expectancies or late in life health of chickens (they don’t). Meanwhile, the yeasts are living their best lives. We have taken to calling our current epoch the human epoch, the anthropocene, but it probably makes more sense to note the influence of our overlords. We live in the yeastocene, an epoch in which single-celled fungi exert startling and disproportionate influence. In our complex mutualism, their lives have benefited far more than our own.
The good news is that the yeasts have tricked us by taking advantage of our ancient preferences. As Monica Sanchez and I argue in Delicious, they appeal to our sweet taste receptors and, often, our sour taste receptors too. They can also produce complex aromas (AKA, bouquets); some scholars argue that humans have an innate preference for such complexity (and that such preferences may have led us to fire, cooking and fermenting in the first place). And, via mechanisms we don’t yet fully understand, they make us feel good and, at least some scholars have argued (Slingerland 2021), make us better able to tolerate each other at the high densities at which we now live than would otherwise be the case. They make us feel happy even if we aren’t always well, which is something to which we might drink; a toast then “to the overlords,” who have long had the last say.