Pre-Agricultural Nutrition

I have seen exaggerated dietary claims based on evolutionary reasoning from different viewpoints, vegans claiming it shows we were herbivores, paleo advocates that we evolved eating a lot of meat, and low-carb advocates that we evolved for a million years eating low carb. The truth is a bit murkier, as we’ll see. Exactly what we evolved on is controversial. But it is clear from the fossil record that pre-agriculture hunter gatherers were robust and in good health, and I think a lot can be inferred about healthy eating from their various diets, which ranged from high plant content/low animal to low plant/high animal, depending on the environment they were in.

For about 99% of our evolution, humans were primates, eating a diet with a very high percentage of plant foods [1]. The first Humans (Homo Sapiens) appeared about 200,000 years ago in Africa, and spread to the four corners of the earth by about 40,000 years ago [2]. Homo Sapiens are omnivores but are more anatomically similar to herbivores than carnivores: we have alkaline saliva, with salivary amylase to digest starch from plant foods, much longer digestive tracts than carnivores [3], and much longer food transit times (carnivores have much shorter transit times to prevent putrefaction of meat). There have been counter-arguments about the human digestive tract vs carnivores [4], but flaws have been pointed out in the measurements used, and upon closer examination the human digestive tract appears to most closely resemble that of frugivores (fruit eaters) [3], which makes sense since other primates eat diets high in fruit.

We do have some distinctions from herbivores, for example we are poor at synthesizing the amino acid taurine, which is a carnivore trait because taurine is readily available from animal sources [5].  Other examples include different populations having different numbers of copies of a gene that involved in digesting starch: “individuals from populations with high-starch diets have on average more AMY1 copies than those with traditionally low-starch diets” [6]. These appear to be more like “tweaks” to our basic anatomy that allow us to eat meat. [update 04/27/21:] But there is one significant piece of evidence of anatomical changes as an adaptation to meat eating: humans have a larger ratio fo the length of the small intestine than that of the colon compared to other primates

An important controversy is over what type of food “made us human”. This dispute is over what enabled the large expansion in brain size that occurred in our hominid ancestors over a few hundred thousand years, leading to Homo Sapiens. It is well accepted that since a larger brain requires a lot more energy, our ancestors probably found a novel source of calories.

The two main candidates are meat [4] and cooked starches [7], especially tubers [8]. Humans have much smaller jaw muscles than other primates, and are missing the sagittal crest on our skulls to anchor larger jaw muscles. It seems reasonable to assume this is because humans no longer have to chew for hours on raw starchy foods, as other primates do. Instead, cooking “predigested” starch for us [9]. That is a controversial point, and I’m not sure what percentage of evolutionary biologists believe that the novel food source that accounts for the evolutionary brain growth was meat or cooked starch, or a combination.

But I don’t think the paleo diet needs to be based on how we evolved. Instead, in my opinion, the most compelling argument is to examine the apparent health as well as the diet of hunter gatherer populations before the invention of agriculture. When Homo Sapiens left Africa and spread all over the planet, it was during the last ice age, so places like Europe and North America were cold and had large mammals, and the inhabitants adapted to hunting. The fossil record for robust hunter gatherers is largely from this period [2].

As for the composition of the pre-agricultural diet, examination of coprolite, or fossilized feces (sounds like a fun job) shows hunter gatherers had a high fiber diet, so they consumed a lot of plant foods. They could also have eaten a lot of animal foods as well, that is not conclusive from the fossil record. Many wild plant foods are highly fibrous but not calorically dense, so a high plant food volume could have been eaten without necessarily contributing a high percentage of the calories in the diet. I’ve seen estimates of a fiber content of as high as 100 grams/day, but if you got that from a high-fiber plant food equivalent to endive it would only require about 550 calories.

Fossil evidence shows that these people were lean, fit, and robust, with no “diseases of civilization”. In contrast, evidence from agriculture civilizations often show shorter stature and poorer teeth, and evidence of deficiency diseases [2]. The agricultural people may well have been protein deficient and had very little variety in their diet compared to hunter gatherers. Clearly, switching from a diet with a variety of nutritious plant and animal foods to one that relied on a few staple foods like grains, with inadequate protein, as was done in cultures practicing intensive agriculture, was not a good move from a health standpoint. So it is reasonable to argue that relying on foods like grains as the staple of the diet is not optimal for health. But I have not seen evidence from the fossil record, nor from contemporary hunter-gatherers, of longevity past 60 on a hunter-gatherer diet. That does not mean it is not possible, with access to modern medicine to address infectious disease and infant mortality, but there are apparently no data to prove it.

[Update 03/10/21]. There is evidence that the Hadza, a hunter-gatherer population living in Tanzania that eat a diet comprised of about 30% meat and 70% plant foods (which are high fiber and a very wide variety), lived to more than 70, and have low incidence of chronic modern diseases.

There is a fascinating history of hunter gatherers in North America in The Art and Science of Low-Carbohydrate Living including the “bison people”. Eating a diet high in meat, low in carbs, and without enough fat, if not done properly, can lead to a deadly condition called protein poisoning (also known as “rabbit starvation” or “Mal de Caribou”). This can happen in cold climates, especially in the winter when not enough plant foods are available, if the animal sources of food are too lean. The bison people made ingenious adaptations to obtain enough fat. There is also a description in the book of a valuable trade good, candlefish oil, which was harvested along the Pacific coast for at least 10,000 years, and had a fatty acid profile as healthy as olive oil. We also know that Native Americans relied on pemmican, a high fat food made from meat and animal fat. This was also an important trade item. From these examples and similar ones from Europe, it is clear that ancestors from this period in colder regions were getting a lot of calories from animal foods. But in the same era, those in more temperate or tropical locales adapted to eating less animal foods and more plant foods [10].

The authors of The Art and Science of Low-Carbohydrate Living make a claim that as far as I know was speculation not backed by data, that since fat was prized, the “bison people” would have eaten mostly the fat from the bison they caught, and not the lean meat, so they had a high-fat diet. I think it is much more likely fat was prized because they were by necessity eating a high-protein low carb diet, and would want to get enough fat to prevent protein poisoning. Also, having discussed the evidence of the bison people, who lived tens of thousands of years ago, the authors claim that a low carb diet is what we evolved on for a “million years”. That is quite a stretch. Our ancestors evolved on the African savanna. Citing evidence of what some of them ate hundreds of thousands of years later during the ice age after migrating to North America is not support for what our ancestors evolved on.

Estimates of the Paleo Diet From Contemporary Hunters and Gatherers

Further evidence about hunter-gatherer diets comes from examining the diets of hunters and gatherers still following their traditional lifestyle in the modern world, which were more prevalent as late as the 1970s [10].

Drs. Boyd Eaton and Melvin Konner published a paper on paleolithic nutrition in 1985 which estimated the average hunter-gatherer population consumed about 35% of their calories from animal foods, 65% plant. This was based on data in the Ethnographic Atlas, a database on 1167 societies, published by George P. Murdock in multiple installments in the journal Ethnology from 1962 to 1980 [11]. In addition to the average, they estimated a variation of percentage of calories in the diet of different societies from 90% plant/10% animal to 10% plant/90% animal depending on the environment [10].
The most interesting contrast is between aboriginal people in Australia living near the coast, who ate a diet much higher in animal foods and lower in plant foods, and their genetically-identical cousins in the interior, who ate much more plant foods and less animal foods.

Dr. Loren Cordain made a detailed statistical analysis of the data in the Ethnographic Atlas and came up with a different estimate, that most hunter gatherers societies would have gotten more than 50% of their calories from animal foods, and would have consumed a relatively high amount of protein and lower amount of carbohydrates [12].

Using the data in the Ethnographic Atlas for the purpose of estimating diet is controversial: it was “written by ethnographers or others with disparate backgrounds, rarely interested in diet per se or trained in dietary collection techniques.” [1]. Also the results in the atlas could have been skewed “because most of the ethnographers were male, they often did not associate with women, who typically collect and process plant resources”, and most hunter-gathering societies remaining by the 20th century “had been displaced to marginal environments.”

[update 05/12/21] I think the best estimate would be evidence of what was eaten on the African savanna around the time human ancestors were evolving big brains. The closest hunter-gatherer society remaining to those conditions are the Hadza in Tanzania, who eat a diet of about 30% animal products, with the remainder of their food coming from an astonishing variety of plant sources that makes their diet quite high in fiber.

The evidence in support of any single version of the paleo diet is controversial. I think it is more widely agreed that there were a variety of pre-agricultural diets, ranging from higher meat in colder regions to higher plant sources in more temperate zones. It is likely most of these diets included:

1. A variety of plant foods.
2. Minimal consumption of grains: grains such as wild rice in North America and wild barley and oats in prehistoric Greece [14] were available, but would have been harder to gather, so probably would have made up a small percentage of the diet. I watched a video reenacting how Native Americans gathered wild rice from canoes. It was a time consuming process.
3. Little or no dairy.
4. Animal foods including meat, eggs, fish, and insects. Meat from wild game would have been much leaner than modern domesticated animals and had a better fat profile (see previous discussion of Omega3). Paleo authors recommend grass-fed beef and pasture raised chickens to address this, but the fat content is still higher than wild game. However, the counterarguments are that organ meats would have been a prized source of fat, and the ingenuity describe above to obtain sufficient fat [13].

Some paleo authors claim that legumes were not consumed in pre-agricultural societies but there is plenty of evidence to contradict that, including lentil and pea consumption in prehistoric Greece [14],  substantial consumption of tsin beans by the !Kung in Africa [15], and acacia seeds (which are a legume) by Australian aborigines [16], and fossil evidence of legume consumption on Neanderthal teeth [17].

It seems you can be eating a variety of amounts of plant and animal foods and still be “eating paleo” (following the dietary pattern of pre-agricultural hunter-gatherers).  This is also discussed in detail in Rob Wolfs’ book Wired to Eat. My fellow blogger at NativeFitness has a lot of useful insight on paleo eating also. He and I agree that beans are a healthy paleo food, he calls them ” vegetarian  meat”, I like that term.

Small Scale Agriculture

The advent of agriculture in many regions of the world spawned civilizations based on large scale farming. These often relied on few, or even one, staple of the diet (“daily bread”, corn, etc.) and had little variety, and were probably deficient in protein. And this led to poor health compared to hunter gatherers.

But some populations continued their hunter-gatherer lifestyle, supplemented by small scale agriculture, so they still got plenty of protein and a good variety of food sources. Examples include Native Americans growing some maize or planting orchards, or other cultures planting tubers. The evidence is that these cultures were just as healthy as hunter gatherers [18]. And most of the rural “blue zone” populations in the world today, that experience the best health and longevity known, also practice small scale agriculture [19]. This may be considered “eating early neo” instead of “eating paleo” but it is still healthy. The Ikarians are a good example of this, they cultivate some foods but also gather an astonishing variety of wild greens, and get a considerable amount of protein from fish.

Is it All a Paleofantasy?

The paleo diet has been criticized by some evolutionary biologists recently. Dismissing it as a “paleofantasy” seems a bit harsh, but they make some valid points, especially about the assumption that there is only one version and it has no grains, and no legumes.

Paleofantasy is the title of Dr. Marlene Zuk’s book. If you read the book carefully she does not dismiss the whole concept of getting clues about what might be healthy by examining what hunter gatherers ate. But she has three main objections:

• Some proponents of the paleo diet present a single, typically high meat, version of the diet as the universal ideal diet. She points out that there were many varieties of hunter gatherer diets.
• She objects to viewing the advent of agriculture as a disaster and what she sees as the fantasy of abandoning civilization and returning to the hunter gatherer lifestyle. She argues there was no point in the past at which we were perfectly adapted to the environment. But despite this objection she does agree that “the past can inform the present” so we can get clues for healthy eating from what worked well in the past vs what is not working well now, like modern processed food.
• A main basis of the paleo diet is the “discordance hypothesis”, originally proposed by Dr. Boyd Eaton [10], that all the lifestyle changes that have occurred since the advent of agriculture and civilization were very rapid on an evolutionary time scale, and that we have not had time to evolve to them. We evolved to be the guy with the spear in the cartoon above, but in the blink of an eye we’re hunched over the computer or worse yet, sitting in a lazy-boy recliner eating junk food. But actually organisms can adapt quickly when their environment changes, which is Dr. Zuk’s specialty. She gives some fascinating examples of rapid adaptation to environmental changes in insects and animals. As for humans, there are multiple cases like a genetic variation that allows some of us to digest lactose as adults, and the adaptation to resist malaria, that have occurred after the advent of agriculture.

But I don’t think the fact that we have done some evolving since 10,000 years ago invalidates the paleo idea. She points out elsewhere in the book that evolutionary changes are often not perfect designs, but compromises. Our spines show evidence that they evolved at a time when we were still knuckle draggers (actually they also have features dating back to fish). They are not ideally suited for us to be upright which can lead to back issues, but becoming upright was an evolutionary advantage.

Another good example of a compromise is the adaptation to malaria in Africa, the sickle cell mutation. If you get one copy of the sickle cell gene it makes you more resistant to malaria, but if you get two copies, it causes sickle cell anemia, a terrible disease. This is clearly not a perfect solution but a compromise. But to me these examples still make the discordance hypothesis valid. Yes it is possible for us to evolve so we would be better able to digest twinkies, but that adaptation would likely be a compromise with side effects. Isn’t it better to just eat healthy foods and avoid the need for that adaptation?

Dr. Zuk also makes a distinction between horticulture and intensive agriculture: We didn’t go straight from being hunter-gatherers to living in cities eating mostly bread. There were hunter-gatherers who remained healthy and fit, who supplemented their diet by planting some tubers or other small crops with sticks. I discussed this above under “small scale agriculture”.

The Paleo diet was also discussed in an interesting Ted talk by Dr. Christine Wariner. She too objected to the paleo diet being in the sole form of high meat, and argued that the fossil record does not support this: hunter gatherers instead ate a variety of foods both seasonally and depending on their region. She also made an interesting argument that the modern versions of foods that are allowed on the paleo diet, like veggies and fruits, bear no relation to their wild Paleolithic predecessors. Some of the salad greens we eat, for example, are bitter and almost indigestible in their wild state. Wild almonds are poisonous (contain too much cyanide). She wondered why we are allowed to eat modern versions of foods like these, highly modified by centuries of farming practices, and call that paleo.

She concluded with some lessons we can learn from what the fossil record does show: There is no one correct diet, but we should eat a diverse amount of whole foods (such as a variety of fruits and veggies), and avoid processed foods. This is not incompatible with a more flexible definition of paleo (or the no-junk guidelines).

My conclusion is there is plenty of evidence that the diet of pre-agricultural hunter-gatherers made them healthy and robust, and there are good nutritional lessons to be learned from it. There was no single diet, people adopted to various healthy ways of eating depending on the environment they inhabited. But it was probably universal that they ate few grains and little or no dairy.

References

1. Milton, K, “Hunter-gatherer diets- a different perspective”,The American Journal of Clinical Nutrition, 2000
2. Eaton, S, Shostak, M, and Konner, M, The Paleolithic Prescription, Harper and Row, 1988
3. Hladik, C, “The human adaptations to meat eating: a reappraisal”, Human Evolution, 2002
4. Aiello L, Wheeler P., “The expensive-tissue hypothesis: The brain and the digestive system in human and primate evolution”. Current Anthropology, 1995
5. Cordain, L, The Paleo Diet, Wiley, 2002
6. Perry, G, et al, ,”Diet and the evolution of human amylase gene copy number variation”,Nature Genetics, 2007
7. Hardy, K, et al, “The Importance of Dietary Carbohydrate in Human Evolution”, Quarterly Review of Biology, 2015
8. Marlowe, F, Berbesque, J, “Tubers as Fallback Foods and Their Impact on Hadza Hunter-Gatherers”, American Journal Of Physical Anthropology, 2009
9. Wrangham, R, Catching Fire: How Cooking Made Us Human, Basic Books, 2009
10. Eaton S, Konner M, “Paleolithic nutrition. A consideration of its nature and current implications.”, N Engl J Med., 1985
11. Murdock G, “Ethnographic atlas: a summary.”, Ethnology,  1967
12. Cordain, L, et al, “Plant-animal subsistence ratios and macronutrient energy estimations in worldwide hunter-gatherer diet”, AJCN, 2000
13. Phinney, S, Volek, J, The Art and Science of Low Carbohydrate Living, Beyond Obesity LLC, 2011
14. Grivetti, L, “Mediterranean Food Patterns”, in The Mediterranean Diet: Constituents and Health Promotion, Matalas, et al, eds, CRC Press, 2001
15. Lee, R, The !Kung San: Men, Women and Work in a Foraging Society, Cambridge University Press, 1979
16. Lister, P, et al, “Acacia In Australia: Ethnobotany And Potential Food Crop”,  In: J. Janick (ed.), Progress in new crops. ASHS Press, 1996
17. Henry, G, et al, “Microfossils in calculus demonstrate consumption of plants and cooked foods in Neanderthal diets (Shanidar III, Iraq; Spy I and II, Belgium)”, PNAS, 2011
18. Zuk, M, Paleofantasy: What Evolution Really Tells Us about Sex, Diet, and How We Live, W. W. Norton & Company, 2014
19. Buettner, D, The Blue Zones: 9 Lessons for Living Longer From the People Who’ve Lived the Longest, National Geographic, 2012