Here Katie shares data describing patterns of fermented food consumption in primates and link it to the existing fermentation literature to provide new insight into the evolution of fermented food consumption by humans.
Editors note: This publication contains the video of the talk from the Fermentology webinar series, as well as a lightly edited transcript of the lecture.
Image attribution: Holtocw (CC BY-SA 4.0).
Today, I want to share where my research has taken me, and what I think are some of the exciting new areas of investigation that we should be thinking about moving forward. I want to start by talking about the relationship that humans have with fermented foods, and how it seems to be unique compared to other animals.
Some non-human animals are documented to consume fermented foods, but it appears to be somewhat infrequent, and limited to a narrow range of foods. In contrast, essentially every human culture incorporates fermented foods into their diets in some way and the diversity of foods that are consumed is immense. All different types of foods are fermented. Of course, beyond just consuming fermented foods, humans also carry out direct fermentation. They intentionally produce these fermented foods for consumption.
As a part of this unique relationship that humans have with fermented foods, it's perhaps not surprising to learn that humans have some adaptations associated with the consumption of fermented foods. Now, these technically aren't unique to humans. These are adaptations that are shared with African apes as well. In particular, there's two genes that we know about that signal this kind of special relationship with fermented foods among the great apes.
The first is the ADH4 gene. We have a special variant of this gene.1 It's an alcohol dehydrogenase gene. It basically lets us break down alcohol more effectively than many other primates. Alcohol is a byproduct of many types of fermentation. There are three major types of fermentation, two of which produce ethanol as a byproduct. Therefore, being able to break down ethanol provides us with an advantage in terms of being able to consume fermented foods.
The other gene is the HCAR3 gene. This gene codes for a receptor that's thought to make humans and great apes more sensitive to signals that come from certain types of microbes, particularly Lactobacillus. Lactobacillus are one of the key groups of microbes that are involved in food fermentations. Together, these two genes suggest that there's a kind of unique relationship between African apes and humans, and fermented foods.
Given this unique relationship between humans and fermented foods, the key questions are: When did it emerge, and why? There's a rich archeological body of evidence that has tried to determine the earliest date that humans have been documented to be using fermented foods. The answer is that it depends on where you are and what you're using as evidence.
There's evidence from Greece that fermentation of grains was being practiced from 4,300 BC. In Southeast Asia, Southwest Europe, and Northern Africa, there's evidence that fermentation was being used from about 7,000 to 6,500 BP. In this case, we're looking at pottery shards that are associated with vessels that are thought to be associated with fermentation of dairy products. If we go even later, there's evidence that has come relatively recently from Sweden suggesting that there was fermentation of fish happening. The fish were buried in pits and probably fermented there. Finally, preserved marula fruits found in caves in Zimbabwe that were used approximately 12,000 years ago suggest long-term storage, and presumably fermentation, of this food. So we can get relatively far back in the archeological record in terms of associating humans with fermented food consumption.
The archaeologist John Speth has posited that there might have even been earlier associations between humans and fermented food use. If so, Neanderthals could potentially have been using fermentation to preserve meat and other types of foods as well. We don't necessarily have the archeological evidence for that though.
If we go beyond the archeological record and actually look at those gene variants I was talking about that appear to be adaptations for fermented food consumption, those genes actually emerged 10 million years ago. This would have been much earlier than the archeological record points to — or can even record. We don't have material evidence from that far back. This is a potentially really ancient association between the common ancestor of humans and great apes and fermented foods.
Another question then is: Why? Why did this relationship emerge so early on? There are a few different ways that we can think about this question.
If we think about the archeological record, and what has traditionally been considered in terms of what we know about material and history, one of the key reasons that's been put forth is food preservation. Fermentation is an effective way to preserve food.
The microbes associated with the fermentation process can outcompete other microbes. They create byproducts that continue to keep other microbes out of the food. These byproducts essentially prevent the food from rotting over time. Specifically, as they ferment the food these microbes create short chain fatty acids, which lower the pH of the food. This acid environment makes it really hard for a lot of other types of microbes to exist and to survive there.
After a while these byproducts even make it difficult for the microbes doing the fermenting to survive. They eventually die-off as well. It really is an excellent food preservative.
Another hypothesis that has been put forth for why this relationship between humans and fermentation emerged is that we like ethanol. We have this kind of affinity for ethanol. In addition to liking ethanol and the intoxication that comes from it, it also helped facilitate social rituals as humans started to settle in communities that were less mobile, and they started to group together in bigger groups. Fermenting foods, and then drinking the ethanol that came from these fermentations, could actually help create community.
One thing to note about both of these hypotheses is that they both rely on technology that allows people to store the fermented foods. Essentially, you need a receptacle in which you can store the food that you're preserving, or store the ethanol that you want to drink later. Therefore, both of these hypotheses narrow our understanding of when our relationship with fermentation emerged to the evidence in the archaeological record for when we know that technology existed in the human species.
There are other potential benefits of food fermentations, however, that don't rely on this sort of technology. In particular, fermented foods are known to have health benefits, both in terms of nutrition, and in terms of probiotics and prebiotics. Nutritionally, fermented foods have higher caloric value than other types of foods. They have higher free amino acid content and to some extent even have higher vitamin content.
Fermentation is also known to degrade fiber and toxins. For example, people that have a gluten allergy sometimes find that they're able to consume things like sourdough bread, because the fermentation action of the microbes can actually break down some of the gluten compounds before the people consume it. The food essentially gets predigested, and it's then less of an allergy issue for the person eating it. We also know there are foods such as blowfish and cassava that need to be fermented before they can be consumed, otherwise, they're toxic, and can really do some damage to people.
As we can see, there are therefore these really great nutritional benefits of fermented foods. Of course, microbes are doing the fermenting of these foods. Fermented foods are therefore, by nature, probiotics. They contain live microbes that can be inoculated into the body.
We know that microbes can affect the nutrition of the animals that they're associated with, the immune function, and the behavior. The byproducts of microbial fermentation, like these short chain fatty acids I referenced earlier, are also known to affect all sorts of aspects of physiology of the animals that consume them, or that have them produced inside of them. Short chain fatty acids can interact with the host’s nutrition and their immune system — even their nervous system.
Given these health benefits, either nutritional or otherwise, which don't require food storage or ethanol storage technology, it seems like the reason humans associated with fermented food so early on in our evolutionary history probably has something to do with these health benefits. But that's really easy to sit here and argue. And the question is: How do we test this idea?
This is really tricky, actually. Ancient evidence is hard to find. So potentially, there's no materials associated with fermentation. There might be vessels and things that are used to store foods and ethanol, for example.
However, as we saw with the fish pits in Sweden, for example, you don't necessarily need those types of recipients in order for food to ferment. In fact, things like fruit ferment naturally in nature all of the time. It doesn't necessarily mean that people are not consuming fermented foods if you don't find the technology associated with it.
Additionally, because fermented foods are potentially easier to digest than other types of foods, there's not really a lot of anatomical or physiological adaptations that are required for consuming them. We can look to some of the genes I already talked about, but we would expect there to be a limited number of genes that we can look at in terms of trying to find the biological evidence. Finally, the biological or chemical residues associated with fermentation are not necessarily unique, and may not preserve all that well.
Now, these are all definitely challenges, and there are people that are working on these challenges. The answer to this may change in five or 10 years, but for now, it's really difficult to look for evidence, at least in these kind of deep evolutionary timelines.
Modern evidence also has its challenges. If we think that our common ancestor with other great apes were using fermented foods to the extent that we have these gene variants and these adaptations to fermented foods, we wouldn’t expect to see a lot of current variation in those adaptations in modern human populations. All humans are probably going to have those adaptations, because we all evolved from that last common ancestor. So it's really hard to look at this across human groups as well.
This is where I would argue that extant primates actually offer a really interesting window into this problem. While it won't give us complete resolution on these questions, if we can determine how pervasive the consumption of fermented foods, particularly late stage fermented foods, is by wild primates, and the ecological context in which it occurs, then we might be able to start to think about some of the ecological and evolutionary forces that could have driven it in humans. We could then contextualize it within human evolutionary history.
To that end, I did an analysis where, together with more than 40 other primatologists, we compiled qualitative data describing overripe fruit consumption from primate field studies around the world. We didn't have chemical data to assess the extent to which these foods were actually fermented chemically. Therefore we were relying on observations, and saying, “That was clearly an overripe food” if it smelled fermented and was very obviously late stage fermented and being consumed by these primates.
Working together, we were able to pull together data from 40 species of primates from 50 research sites around the world. These primate species represented 11 of the 16 primate families. The sites were on all continents the primates inhabit. The habitats encompass both tropical and temperate climates.
We had researchers describe the types of presumably fermented foods that they observed them consuming, the frequency of their use, and any other associated behaviors. We also had everybody provide us with a whole range of information about the sites and the primates themselves. We ran generalized linear mixed models to look at the relative importance of these different variables.
Below is a list of the variables we were looking at. We considered factors that we call socioecological traits, factors that had to do with the primates themselves:
What was their diet?
How big is their body size?
How big are their brains, relatively speaking?
We also looked at climatic data (ie. rainfall, temperature, elevation, latitude, longitude).
Finally, we used habitat size as a rough measure of habitat quality to try to understand how fragmented the site might be.
We then accounted for sampling effort, essentially how long the primates were observed for. All of the studies of primate groups we considered lasted at least nine months and the median study length was 15 months.
We found 15 primate species, which is a little bit more than 1/3 of the species we had data from, that clearly consumed late stage fermented foods. The foods were overwhelmingly fruit. Presumably, this is because fruit ferments easily in nature, and it was also easy for us to observe. It's much harder for us to observe fermented nectar, even though it may (and likely does) exist in flowers that some of these primates consume.
There was no clear phylogenetic bias. Primates all across the order were observed to eat fermented foods, as well as all across the world at about 23 study sites in 12 countries. Generally speaking, there were a large variety of fruits that these primates were observed consuming in these late stages of fermentation.
There's a few primates, such as spider monkeys (Ateles geoffroyi) and capuchins (Cebus imitator), that are consuming seven, eight, or even nine types of fermented fruits. However, most of the primates consume between one and three different species of fermented fruit. Therefore, for these primate species fermented fruit consumption was really limited, generally speaking, to a small subset of fruits.
Another aspect we looked at was the time the primates spent feeding on these fermented foods. Generally speaking, it was a very small amount of the total feeding time during a given year, so anywhere from 0.1% to maybe 5% of total feeding time. However, in some cases, such as with the white-faced capuchins (Cebus imitator) and the brown howler monkey (Alouatta guariba) up to 15% of their feeding time was dedicated to a food item during a specific season when it was available.
The context in which this happened tended to vary. In some cases, this was observed after a patch had been depleted. For example, orangutans would consume overripe fruits if there were no other fruits left in that fruit patch. For the brown howler monkey and the spider monkey at two sites, this type of behavior occurred during periods of altered food availability. So there wasn't as much as the preferred food available.
Another interesting thing to point out is that 31 of the 44 fruit species that were reported to be consumed in this late stage of fermentation appear to have some sort of defense against herbivores. These could be physical defenses, like a tough husk, or skin that's really hard to break into, or they could be secondary metabolites, like alkaloids, acetogenins, saponins, and tannins — things that would otherwise deter these primates from consuming them. It is possible that fermentation is allowing the primates to take advantage of some of these fruits, because it's breaking down some of those physical defenses and those toxins.
I also wanted to point out that there were a few reports of preference for fermented foods and possibly even incitation of fermentation. Spider monkeys, white-face capuchins, and brown lemurs were all reported to actually actively knock fruits out of trees of a specific species, and then eat them off of the ground sometime later.
In the case of the white-faced capuchin, the capuchins would knock fruits to the ground and then they would come back up to two weeks later. They would not consume these fruits unless they were fermented. The fruits on these trees had really tough outer husks so the capuchins essentially couldn't get at the fruit unless it was fermented. The spider monkeys and the brown lemurs would consume the fruits when they were not fermented. However, in the case of the lemurs, for example, they would eat the fruits off the ground first if fruits were available both on the ground and in the trees. This is just some evidence that there may be a preference for some fruits to be consumed fermented, even when regular ripe fruits are available. There may actually be some purposeful behavior occurring here, although that's speculative.
The last thing I wanted to point out is from our models: there were a few key variables that came out as significant predictors of fermented food consumption. Our positive predictors were mean annual maximum temperature and habitat size. The hotter and bigger the habitat, the more likely fermented food consumption was. The negative predictors were mean annual minimum temperature and rainfall. Essentially, the higher the annual low temperature, the less fermented food you saw, and the less rain there is, the more fermented food consumption we saw. Therefore, the environments that are more extreme in terms of temperature and rainfall were the environments in which we saw the primates engaging in this behavior more often.
This pattern could be a result of the primates being able to find the fermented foods. Perhaps in hotter temperatures foods ferment more readily and/or it's easier to smell the ethanol that's evaporating from them. Perhaps some of these plants are actually more defended, whether it's physically or chemically, and the primates actually need to rely on fermentation to be able to access some of these fruits in these habitats. Those are open questions.
The overall finding from this analysis was that, first of all, fermented food consumption is pretty widespread in non-human primates, though certainly not to the degree that we see in humans. If you think about it, we're looking at this late stage fermentation and there are other foods that we weren't able to detect because we didn't analyze them chemically. Therefore this is not necessarily an uncommon behavior in non-human primates, but again, it's not as frequent, and it doesn't involve as diverse an array of foods as it does in humans.
To the point about the health benefits of fermented food, it really does seem that the use of targeted consumption of fermented foods by primates may be part of a broader nutritional strategy to increase food availability and expand the dietary niche. Whether primates are using fermented fruits as a kind of fallback food, eating them when other foods are not available or when they've gotten to a patch too late, or they're consuming them because that particular food would not be edible unless fermentation has broken down some of the plant defenses, it seems to be part of some sort of dietary strategy.
If we go back to thinking about human evolution, it's possible that, as with other primates, fermented foods were eaten by humans as fallback foods during human evolution. This has actually been suggested by Matt Carrigan and the other authors of the paper that presented the variation of the ADH4 gene. Fermented foods also could have increased edibility of things like underground plant storage organs that we think some of our human ancestors relied on relatively heavily as we started to inhabit more open environments.
I'd also argue that we should think about this in terms of grains. Wild grains tend to be high in toxins and fibers. Fermentation may have actually been necessary to make them more edible. Some of this archeological evidence that we see associated with grains we think may be a signal of ethanol production, could also have just been a fermentation process to make the grains themselves edible. The ethanol content would just have been a kind of side effect. Of course, I haven't even touched on the other potential health benefits that could be associated with these fermented foods because of their probiotic or prebiotic properties. However, that's much harder to address with the data we have right now.
Some key considerations that I think we should start integrating into our perspectives on human evolution and fermented foods is, first of all, humans don't need specialized technology to consume fermented foods. We see this sort of behavior happening in non-human primates without any of the types of technologies that we usually associate with fermented food consumption, but also production. If we consider a capuchin knocking some of these foods out of the trees and coming back later as a purposeful act, we could argue that the same sort of thing could have been occurring early in human evolutionary history.
I'd also like to suggest that the consumption and production of these foods could have increased human dietary niche plasticity, allowing humans to consume food items they wouldn't have been able to consume otherwise, potentially because of toxins and other sorts of plant defenses. Alternatively, it may have allowed them to inhabit seasonal environments, and use fermented foods as a fallback food. In this case, without these foods, they wouldn't have been able to survive in those environments otherwise.
The energy and nutritional benefits provided by fermented foods could have also altered human energy budgets, the amount of energy and nutrients that humans could extract from different environments. This could have affected life history processes such as growth and development (for example, brain size, etc.). I would argue that while things like consumption of meat, cooking, domestication of plants and animals have all been really integrated into our consideration of human evolution, and the types of nutritional challenges that humans were likely facing across our evolution, I think fermented foods should also be integrated into these frameworks and theories. We should really start to think about the potential importance of them more critically.
The last thing I just want to put forward is that Old World monkeys were evolving in similar changing environments at the same time as some of our human ancestors. As the climate began to change, we started using more open habitats and woodland areas. Old World monkeys also inhabited these types of habitats. However, we don't see Old World monkeys fermenting foods the way that humans do. That said, cercopithecines, which are one group of Old World monkeys, have cheek pouches that contribute to the predigestion of food. It has been argued that these cheek pouches have evolved as a result of food competition. Essentially, they allow these monkeys to stuff food in their mouth, and then run away and eat it later, avoiding food competition.
These food pouches in their cheeks also have huge enzyme activity, and can break down foods that are in the cheek pouches really, really quickly. There is this kind of pre-digestion fermentation that happens in the cheek pouches. Interestingly, it’s quite analogous to some of the human fermented food practices. So if we think about things like chicha, where people are chewing up foods to start the fermentation process, and then finishing the fermentation process in receptacles, cercopithecine food processing in cheek pouches isn't actually that different than the beginnings of some of the human fermented food production processes.
I think it's really interesting to think about whether directed fermentation by humans and cheek pouch predigestion by cercopithecines could represent similar dietary strategies for these primates that were inhabiting these kind of similar environments that were nutritionally challenging, and may have presented obstacles in terms of seasonality of foods, or the defenses associated with plant underground storage organs. These could actually be convergent strategies.
I'll just throw it out there briefly that to the extent that the gut microbiome tells us something about the physiology and ecology of the host with which its associated , microbiome data from humans, apes, and cercopithecines suggest that there could actually be this sort of convergence.
The gut microbiomes of cercopithecines are more similar to that of humans than other non-human apes. We do think that these microbiome signals are very closely tied to physiology, diet, and ecology. It's interesting to me to think about whether some of this signal of similarity in the gut microbiome could be a result of this kind of convergent predigestion strategy that humans and cercopithecines are engaging in.
So I hope I’ve gotten you thinking about how ancient humans’ relationship with fermented foods may be and how we might go about testing it. There are many unanswered questions still, but I’m excited to see what we learn in this area as we continue to ask them and develop new tools to address them.