The human brain developed thanks to fermented foods
21st February 2024
Translated from the original article in Catalan
Science Alert is a good free scientific newsletter in which every week I find some interesting news. A few weeks ago I was especially surprised by an article (Dyer 2023) on this hypothesis of the title. Apart from this article, to know the details I went to the original publication by Bryant et al. “Fermentation technology as a driver of human brain expansion”, which I will comment below.
LARGER BRAIN
The main distinguishing feature of humans with respect to other primates and other animals is the larger and most complex brain. Because the greater an animal, the greater the weight of the brain, a relative measure is used: the encephalization quotient (EQ), which is the relationship between the mass of the brain and the expected one for a typical animal of the same dimensions. Homo sapiens‘s EQ is around 7.5, while for other primates it is between 2 and 3, and in other mammals like the dog is between 1 and 2, except cetaceans such as orcas or dolphins, which have 3 or 4.
Therefore, the human brain tripled its size with respect to other primates in its evolution since the last Australopithecus —which were already bipedal, and therefore had their hands free— about 2.5 million years ago (Ma) until to the first Homo about half a million years later. The Australopithecus had an endocranial volume (ECV) of 400 mL (Figure 1), while for Homo erectus (Figure 2) it was about 800 mL, and then the expansion of the brain continued with the emergency of H. sapiens and previously with H. neanderthalensis, both with about 1500 mL (Miller et al. 2019; Ponce de León et al. 2021). Obviously, this enlargement of the brain and especially of the prefrontal cortex determined the increase in the capacities of reasoning, reflection, adaptation, socialization and other skills, that is, of the development of human intelligence.
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MORE BRAIN AND LESS GUTS
There are several theories about the mechanisms that would have favoured this accelerated expansion of the brain. The limiting factor in enlargement is the availability of caloric resources because the brain has a high metabolic spending, compared to most other tissues. The metabolic rate of the brain at rest accounts for 22% of that of the human body (McClave & Snider 2001).
Mutations that led to an increase in brain size, although they would have clear final benefits, would not be adaptive if they had a greater risk of hunger. A reduction in the amount of intestinal tissue, which has metabolic needs like those of the brain, would release calories necessary for digestion to reassign them to the brain. This is confirmed by the fact that the size of the colon of humans is the fourth part of the corresponding to primates of our size (Table 1), while the brain of the current H. sapiens is almost the triple.
Table 1. Expected mass of some human organs based on the values of great apes compared to the real ones of a 65 kg western human (adapted from Bryant et al. 2023).
Organ | Expected mass (kg) | Real mass (kg) | Real / expected |
Heart | 0.32 | 0.30 | 0.94 |
Liver | 0.24 | 0.30 | 1.25 |
Small intestine | 0.40 | 0.62 | 1.55 |
Colon | 0.85 | 0.22 | 0.26 |
Brain | 0.45 | 1.30 | 2.89 |
CHANGES IN DIET
However, this intestinal reduction had to be accompanied by a change in the diet, with easier digesting foods and more energetic ones. The precursor hominids of Homo would have changed from an herbivorous-frugivorous regime to an omnivore-carnivorous one. Until now, the hypotheses point to the following two changes, well known and quite plausible:
1) The higher consumption of meat —of animal protein in general— has been argued as one of the key elements in human evolution. H. sapiens‘s diet is clearly more carnivorous than the other primates’ diet, and therefore the hunting of other animals should have been a growing habit in Homo precursors (Mann 2000). However, a weak point of this hypothesis is that hunting seems to be unimportant initially —circa 2 Ma—, since these first Homo and their precursors were mainly gatherers, and hunting was fully strongly developed later, at the end of the lower Paleolithic —about 500,000 years ago— in parallel with the development of the first prehistoric weapons (Bryant et al. 2023).
However, it seems that the consumption of carrion left by other carnivorous animals was prior to the hunt, from the end of the Pliocene or the beginning of the Pleistocene about 3 Ma. An alternative related to scavenging but more profitable for consuming meat is to take the prey hunted by other animals. In fact, archaeological records show that the latter option for fresh meat was predominant on passive carrion, where meat consumption performance is lower (Bunn & Ezzo 1993).
But the consumption of high nutritional animal protein is not limited to mammalian and bird meat: fishing must be considered and especially seafood harvesting. The latter case has the archaeological advantage of having found many places with mollusc shells accumulation, which indicates the great exploitation of this protein resource by humans since long ago. The oldest found shells are those of Pinnacle Point in South Africa 160,000 years ago, very important because together with other remains they are one of the pieces of evidence of the first Homo sapiens (Marean et al. 2007), but of course, they are certainly later than the brain enlargement.
2) The domestication of fire and the consequent possibility of cooking food was another crucial element to obtain more bioavailable caloric substrates and to digest them more easily, both at the mechanical chewing level and of energy expenditure on the digestive tract. This is very evident in the commented consumption of meat, both fresh and carrion, and in this case to mitigate microbial pollution. In addition, cooking was also very important in allowing the ingestion of vegetable foods and especially tubers, rich carbohydrate reserve organs, but they are not directly digestible and/or contain toxic compounds if they are not cooked (Wrangham et al. 1999).
However, there is no clear archaeological evidence that Australopithecus or the first Homo dominated the fire. The first evidence would be for H. erectus between 1 and 1.5 Ma (Hlubik et al. 2019) but more clearly for 800,000 years ago (Goren-Inbar et in 2004). Therefore, the full control of fire would have been achieved after the beginning of the brain development. In fact, fire expertise requires the cognitive ability to plan, create, maintain and use fire effectively, that is, a brain more developed than that of Australopithecus (Bryant et al. 2023).
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HYPOTHESIS OF EXTERNAL FOOD FERMENTATION, in contrast to the usual “INTERNAL”
The authors of the work (Bryant et al. 2023) propose this term of “external” to differentiate it from the internal fermentation that is made by the microbiota of the human gastrointestinal tract in digestion. The idea is that the outsourcing of this internal fermentation released body energy requirements that allowed cerebral expansion.
It should be remembered that the term “fermentation” is used here in its more general meaning transformation of organic compounds by microorganisms, while the original meaning of the concept of “fermentation” in a biochemical sense is strictly the type of metabolism anaerobic metabolism where energy and carbon source are organic compounds, and the electron acceptor are these same compounds. Most food fermentations such as dairy or alcoholic one belong to this biochemically speaking meaning, but other processes of microbial transformations that we include in addition to these when talking about “fermentation” in general, are other types of metabolism, such as aerobic degradation or other reactions. You can see more information on fermented foods in my post “Fermented Foods: consensus statement and reviewing them” (Figure 3).
Although it is not usual to call it this way, the digestion that takes place in the human gastrointestinal tract or other animals includes this “internal fermentation“, understood as microbial intervention, that is, the set of transformations performed by microorganisms, the intestinal microbiota, especially in the colon. The digestion of a significant part of plant fibrous components requires this internal fermentation by the microbiota. In ruminants this is achieved with additional stomachs and an abundant cellulolytic microbiota. In the other non-ruminant animals, including primates, there is a more developed colon and cecum, and a higher area for the absorption of nutrients. The colon of humans and many primates contains about 10^12 microbes per mL and the transit time for this large gut is about 20-40 hours, while for the small intestine it is only 2-4 h (Bryant et al. 2023). The relevance of the microbiota of the colon for health is becoming clearer, in terms of nutrient absorption, energy regulation and a correct immune system (O’Hara & Shanahan 2006).
Soluble fibre, especially oligosaccharides, is fermented by the microbiota, producing short chain fatty acids (SCFA), which provide about 2 cal/g of fibre, which is an additional 50% to 4 cal/g available for direct digestion of easy carbohydrates (starch, sugars). These 2 cal/g are 2-10% of the total energy that the diet gives us, which is very small compared to other mammals (Table 2). These SCFAs are mainly acetate, propionate and butyrate. Acetate is used to synthesize cholesterol and other SCFAs, and provides energy to the heart, kidneys and muscle; propionate is a precursor to the liver synthesis of glucose and proteins; and butyrate is the favourite source of energy for colonocytes.
Table 2. Energy derived from short chain fatty acids (SCFA) produced by the fermentation of the gut microbiota.
Species | Diet | % Energy of total digested |
Cattle | Herbivorous ruminant | 72 |
Sheep | Herbivorous ruminant | 84 |
Rabbit | Herbivorous monogastric | 32 |
Beaver | Herbivorous monogastric | 19 |
Porcupine | Herbivorous monogastric | 16 |
Pig | Omnivorous | 36 |
Howler monkey | Herbivorous monogastric | 30 |
Gorilla | Herbivorous monogastric | 57 |
Homo sapiens | Omnivorous | 2-10 |
Apart from the SCFA, the main nutrients produced by the microbiota are vitamins B and K, which are absorbed by the gut. In addition, the microbiota increases the bioavailability of mineral micronutrients by degrading antinutritional factors such as phytates and oxalates —present to many vegetables—, which form complexes with cations (Fe, Zn, Mg, Ca, …) and prevent their absorption.
The external food fermentation that the first humans began to perform has similar functions to the internal one, such as increasing bioavailability and absorption of macronutrients and micronutrients. All this increases the digestibility of carbohydrates and proteins, for example in legumes hydrolysing macromolecules to amino acids and more digestible sugars. Carbohydrate fermentation also increases available vitamins B in an order of magnitude (Sandhu et al. 2017). And the phytates and oxalates can be degraded by the phytase produced by lactic acid bacteria present in external fermentations, increasing the absorption of minerals. This elimination of phytates is even more effective by fermenting than by cooking since the activity of phytase decreases above 80ºC when food is cooked.
A great benefit from external fermentation is that it can make toxic food cease to be. The best -known case is the detoxification of the cyanogenic glycosides of the cassava, a basic food of millions of people in tropical areas. If it is not fermented, these glycosides are hydrolysed by the colon microbes producing the toxic cyanide. When cassava is properly fermented by lactic acid bacteria, the cell walls of tubers break and allow toxin hydrolysis, also favoured by the lactic acid produced by these bacteria (Padmaja & Steinkraus 1995).
In addition, external food fermentation contributes to a better efficiency of the intestinal microbiota in digestion. First, part of the microbiota ingested with fermented food can colonize the intestine, contributing to microbiota biodiversity, increasing the ability to ferment more nutrients, and favouring that some endogenous microbes produce bacteriocins against possible pathogens. It has been seen that these benefits are also possible although fermented food microbes have only transitional contact with resident bacteria (Ohland & Macnaoughton 2010). With this, external fermentation can help the endogenous microbiota to protect human host from infections and diseases, because a correct microbiota producing an amount of SCFA from non-digestible carbohydrate fermentation is well related to a reduction in gastrointestinal disorders (Alexander et in 2019).
EXTERNAL FOOD FERMENTATION, DRIVING THE EXPANSION OF THE HUMAN BRAIN
As seen before, it seems that diet changes observed from Australopithecus to humans, such as the highest meat consumption or cooking food with fire, are relatively later than the expansion of the brain, and only with these changes it is difficult to explain the rapid development of the brain, simultaneous with the reduction of the colon and the displacement of high energy expenditure of the intestine to the brain.
For beginning of external food fermentation, it would not need to have a great capacity for reasoning. Australopithecus already had some simple tools that they could use to scorch animal or carrion, and could transport this food to home, being it a cave or a temporary shelter, thanks to the already developed bipedalism. They could also transport fruits, tubers and other potential foods. Although, for example, chimpanzees can occasionally carry temporary tools or the remains of hunted animals, they do it within short distances, about hundreds of meters at most, and most foods are consumed at the capture site.
Once at home, these first Homo probably left some food to consume it later, and surely accumulate more food than the captured. The reusing of storage site would have promoted a microbial ecosystem that would lead to fermentation. Food again incorporated would have been inoculated with those microbes present in the place, or in the body of the same hominids, for example. This socially transmitted practice to reuse sites, containers or tools for manipulating food would have been promoting the fermentations and stability of fermentative microbial agents. As in any selection process, this primitive technology would have been modified, especially learning not to consume the products damaged with toxic pathogens or compounds, probably with some human victim along the way.
This external food fermentation requires little knowledge, much less than the use of fire, since fermentation is a natural process that can pass spontaneously. It is a passive process for which there is no need for active efforts such as maintaining fire. In addition, fermentation can preserve food for a long time, even years, thanks to some fermentation products such as lactic acid or ethanol.
In fact, it is proposed that other species of Homo such as Neanderthals were already fermenting meat, in such a way that the decrease of pH by the acid produced preserved the vitamin C contained in the meat and thus avoided the scurvy (Speth 2019) .
Surely fermentation would be combined with other conservation techniques such as smoking, drying and salting, as it is currently done. The ease of fermentation in very different types of foods, environments and conditions must have been disseminated. The most obvious proof is that nowadays there are multiple fermented foods, in virtually every part of the world. It is estimated that there are more than 5,000 varieties of fermented foods, which are 35% of the current market of all foods, according to FAO. We see some of them in Table 3. We can also see a selection of 36 of them on a gastronomic information website: howtocook.recipes.
Table 3. List of fermented food, sorted by substrate types: vegetable or animal (modified and enlarged from Bryant et 2023).
Product name | Substrate vegetable: leaves, roots | Type of product | Place of origin | Microorganisms |
Kimchi | Cabbage leaves, radish, others | acid | Korea | Lactic acid bacteria (LAB) |
Sauerkraut | Cabbage leaves | acid | Europe | LAB, enterobacteria |
Pu-erh | Tea leaves | acid, beverage | Asia E | Moulds, yeasts |
Kombutxa | Tea leaves | acid, beverage | Asia E | Acetic acid bacteria, yeasts |
Dolma | Grape leaves | acid | Europe SE | LAB |
Gundruk | Leaves of radish, cabbage and others | acid | Nepal | LAB |
Sinki | Radish root | acid | Nepal | LAB |
Garri | Cassava root | acid | Africa W | LAB, moulds, yeasts |
Sapal | Taro tuber | acid | Papua Nova Guinea | LAB, yeasts |
Poi | Taro tuber | acid | Hawaii | LAB |
Tocosh | Potato tuber | acid | America S | LAB |
Fufu | Nyam and cassava roots | acid | Africa W | LAB |
Product name | Substrate vegetable: fruits, seeds | Type of product | Place of origin | Microorganisms |
Natto, Kinema and others | Soybean | alkali | Japan, Asia E | Bacillus subtilis (more info in my post) |
Gochujang | Pepper, rice, soy, cereals | acid + sweet spicy, condiment | Korea | Bacillus, Enterococcus, cyanobacterium Aerosakkonema, moulds |
Tempeh | Soybean | alkali | Indonesia | Rhizopus |
Soy sauce | Soybean | alkali + acid, condiment | Asia E | Aspergillus oryzae (koji), LAB, yeasts |
Miso | Soybean, cereals | alkali + acid, condiment | Japan | Aspergillus oryzae (koji), LAB, yeasts |
Oncom | By-products of soy, cassava and others | alkali | Indonesia | Rhizopus, Neurospora |
Sumbala, Dawadawa | Néré (Fabaceae) seeds | alkali | Africa W | Bacillus, LAB |
Coffee | Coffee seeds | acid, beverage | Africa E | Enterobacteria, Bacillus, LAB and yeasts |
Cacao | Cacao seeds | acid | America central and S | Yeasts, LAB and acetic acid bacteria |
Table olives | Fruits | acid | Mediterranean | LAB, yeasts |
Pickling | Cucumber, eggplant, radish | acid | Mediterranean | LAB, acetic acid bacteria |
Vinegar | Fruits, cereals | acid, condiment | Mediterranean | Acetic acid bacteria |
Sourdough | Cereal grains | acid, dough | Europe, Asia W, America N | LAB, yeasts |
Appam | Rice, coconut milk | acid, pancake | India | LAB, yeasts |
Idli | Rice and lentils | acid | India | LAB |
Kenkey | Maize grains | acid, dough | Africa W | LAB, yeasts |
Pozol | Maize grains, cacao | acid, beverage | America central | LAB, other bacteria, yeasts, moulds |
Injera | Cereal grains (Eragrostis tef) | acid, pa | Ethiopia, Africa E | LAB, Bacillus, enterobacteria, yeasts |
Product name | Substrate vegetable: fruits, seeds | Type of product (alcoholic) | Place of origin | Microorganisms |
Pulque | Sap of maguey (Agave) | alcohol, beverage | Mexico | Zymomonas, LAB, yeasts |
Wine | Grapes, fruit vine | alcohol, beverage | Mediterranean | Yeasts, and LAB in malolactic fermentation |
Cider | Apple | alcohol, beverage | Europe W | Yeasts |
Pear cider | Pear | alcohol, beverage | United Kingdom, France | Yeasts |
Fruit wine | Fruits: cherry, banana, others | alcohol, beverage | Europe N, America central | Yeasts |
Beer | Cereal grains | alcohol, beverage | Europe, Asia W | Yeasts |
Sour beer (more info in my post) | Cereal grains | alcohol + acid, beverage | Belgium, Germany | Yeasts, LAB |
Kvass | Cereal grains | alcohol + acid, beverage | Europe E | Yeasts, LAB |
Sake, rice wine | Rice grains | alcohol, beverage | Japan | Yeasts, Aspergillus oryzae (koji) |
Makgeolli, Korean rice wine | Cereal grains | alcohol, beverage | Korea | Yeasts, Aspergillus, LAB, proteobacteria |
Chicha | Maize grains | alcohol, beverage | America S | LAB, other bacteria, yeasts |
Product name | Substrate (animal product) | Type of product | Place of origin | Microorganisms |
Med, hydromel, Tej | Honey | alcohol, beverage | Africa, Asia, Europe | Yeasts |
Cheese | Milk | acid | Worldwide | LAB, other bacteria, yeasts, moulds |
Yogurt, other fermented milks | Milk | acid | Europe E, Asia W | LAB |
Crème fraiche | Milk | acid | France, Europe | LAB |
Kefir | Milk | acid | Caucasus | LAB, yeasts |
Kumis | Mare milk | acid, alcohol | Asia central, America S | LAB, yeasts |
Chal | Camel milk | acid | Asia central | LAB, yeasts |
Leben | Milk | acid | Africa N, Asia W | LAB |
Buttermilk | Butter | acid | Europe, Asia W | LAB |
Fermented sausages | Pork meat and others | acid | Europe | LAB, yeasts, moulds |
Ham | Pork meat | acid | Europe | LAB, other bacteria, moulds |
Nem chua | Pork meat, rice, banana leaves | sweet-and-sour | Vietnam | LAB |
Satchu | Meat | acid | Himalayas | LAB, other bacteria, yeasts, moulds |
Pemmican | Bison meat, deer, others | acid | America N | Various bacteria |
Dodery | Bones of animals | acid | Sudan | Bacillus, various bacteria, LAB yeasts |
Tiroi | Mussels, other seafood | acid | New Zealand | Various bacteria, LAB |
Kina | Sea urchin | alkali | New Zealand | Various bacteria |
Hákarl | Shark | alkali | Island | Proteobacteria: Moraxella, Acinetobacter |
Ngari | Fish pool barb | acid | India, Himalayas | BL, Bacillus, yeasts |
Surströmming | Herring | acid | Sweden, Europe N | Halanaerobium (firmicute), LAB, other bacteria |
Nam-pla, bagoong and others | Various fishes | acid, condiment | Asia SE, Philippines, Europe | Bacillus, other bacteria, archaea halophiles |
Garum | Fish entrails | acid, condiment | Old Greece, Rome, Byzantium | Various bacteria and archaea |
Fermented foods currently are an important part of the human diet everywhere, both in regions where food safety and conservation are not well controlled but also in more developed countries. It is a global technology among humans, which is a proof that it comes from early humans. As seen (Table 3), food substrates can be vegetable, from the different parts of plants, or from many different animals.
Also, although cultural practices of fermenting foods vary greatly globally, it seems clear that we humans generally like fermented foods. This preference would have emerged in parallel with an adaptive attraction to the aromas and textures of fermented foods by early humans. This is why we can see how many of these foods are condiments, that is, they are added to other foods in order to improve their palatability (Bryant et al 2023).
This great diversity of fermented foods means that some very strange tastes and aromas are highly appreciated by some cultures and detested by others, as is the case with some very smelly cheeses, with volatile ammonia and sulphur compounds. There is a cultural specificity in its consumption. The same aromas that may signal “good” food in one culture may signal bad or stale food in another. The ability to “taste” acidic, sour, or bitter foods —tastes unusual in natural foods and absent in other animals— must have evolved in humans with the production of fermented foods (Frank et al 2022).
As seen before (Tables 1 and 2), the development of external food fermentation was linked to a significant loss of colon mass and of the energy produced there, and therefore this implies a reduction in quantity and diversity of the intestinal microbiota because these are not so necessary. This is evidenced when doing comparative analyses of the human microbiota with that of other hominids such as chimpanzees, bonobos or gorillas (Moeller et al 2014).
On the other hand, the preference of humans for fermented foods is also demonstrated by genetic analyses. For example, some olfactory receptor genes related to fermented products are positively selected in humans and not in chimpanzees, such as methyl octanoate, a fruity odour produced by winemaking yeasts, or methyl valeric acid, a key aroma in ripened cheeses.
The ability to metabolize the ethanol produced in alcoholic fermentation and therefore be able to consume it in moderation is due to gene variants that code for alcohol dehydrogenase (ADH7), which would logically have been promoted in the first humans with the first drinks obtained by fermentation. However, it seems that this ability would predate humans, because other great primates have it, and even other mammals such as some Chiropters. All these are consumers of fruits, which can be fermented spontaneously in nature, and therefore all these animals would have acquired this ability by consuming fruits that have been partially fermented (Janiak et al 2020). So, hominids would already be adapted to metabolize ethanol long before the first humans did it in a more targeted way (Carrigan et al 2015).
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CONCLUSION
I believe that this hypothesis of external food fermentation as a key element in the brain expansion observed in the evolution from Australopithecus to humans is very plausible. Food fermentation in many cases is almost spontaneous, it initially requires very little technology and knowledge, and with a minimal selection of the resulting products after fermentation, more digestible foods are obtained, which are better preserved, and which have tastes or new and interesting textures.
This development of fermented foods allowed not being necessary to have a considerable volume of colon with its diverse microbiota, to acquire nutrients that can be consumed by preparing them beforehand. By reducing the caloric needs of the colon, the “leftover” energy could be devoted more and more to the brain, facilitating its expansion. Logically and in parallel, or in some cases later, the other factors discussed such as the consumption of meat, new hunting technologies, socialization, and fire, allowed even more this enlargement of the brain, until reaching Homo sapiens.
Finally, I just want to comment that I particularly have liked this work because it puts together three of the topics that most attract me scientifically:
1) Fermented foods, or as Bryant et al’s article calls it, “external fermentation.” In fact, this external designation surprised me, since I had never thought of calling “internal fermentation” the set of processes of modification or degradation, or synthesis of compounds carried out by the intestinal microbiota. But ok, it’s true. In any case, fermented foods and aspects of the benefits of microorganisms (“the good microbes”) have always been my primary topic of research work, and teaching, and my interest since I finished my bachelor’s degree in biology 50 years ago.
2) Intestinal microbiota. It has been a topic that has interested me for several years. Although I haven’t worked on it directly at a research level, I have been getting to know it, and I touch at a teaching level. As we have seen in recent years, the role of the gut microbiota in the healthy maintenance of the body is much more important than we thought, although there is still much to be learned. Curiously and somewhat disappointed, I have discovered with this work, that humans have reduced the gut microbiota compared to other primates, precisely with the development of this “external fermentation”.
3) Origin and human evolution. Of course, this topic is of great interest to me, as I suppose to everyone. With a certain knowledge of living beings and admiring how all biological evolution works, knowing more about how our species appeared and those close to us, is exciting.
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BIBLIOGRAPHY
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Posted on 21/02/2024, in Bacteria, Evolution, Genetics and molecular biology, Lactic acid bacteria and products, Microbiota and tagged Australopithecus, bacteria, brain, colon, cooking, diet, digestion, evolution, fermentation, fermented foods, gut microbiota, Homo, Homo erectus, Homo sapiens, human, human evolution, internal fermentation, lactic acid bacteria, meat, microbiota, yeasts. Bookmark the permalink. 1 Comment.
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