Bipartisan Alliance: 03/07/19

Ben-Dor, Miki (2019) "How carnivorous are we? The implication for protein consumption," Journal of Evolution and Health: Vol. 3: Iss. 1, Article 10. https://doi.org/10.15310/2334-3591.1096

Full text, references, etc., in the link above.

Introduction
The Paleo Diet evolutionary mismatch principle suggests that the closer we stay to the diet that we evolved to consume the better chances we have to stay healthy. There is little doubt that meat was a significant component of the Paleolithic diet and that it was acquired largely by hunting [1] and thus Paleolithic humans can be defined as carnivores.The definition of carnivory, however, is vague as a dietary pattern. There are 'carnivores' belonging to the Carnivora familythat doesn't eat meat (Panda bears).There are 'obligate carnivores' that rely on very high protein consumption (cats).There arehypercarnivoresthat by definition consume more than 70% of the calories from animal sources and there are even 'epic carnivores 'at the very top of the food chain (lions). The purpose of the present investigation is not to assign humans to any of these categories but to find out whether during our evolution we became adapted to consume large quantities of meat on account ofaprevious adaptation to consume large quantities of plants. If so, we can assume that a relativelylarge quantityof meat will be safer than consuming a relativelylarge quantityofplant foods. Another question that comes up is to what level of protein consumption we became adapted. Since in diet, every item that we consume replaces anitem that we could consume, if we are adapted to consume animal sourced protein, we can consider it to be a safer food than other foods, like domesticated plants, In this context, the question of the evolutionary level ofprotein consumption during the Paleolithic has never received adequate attention. Since there is relatively little protein in plants, the answer is derivedfrom the relative amount of animal food in the human diet.If animal food consumption wererelatively high during the Paleolithic,then relative protein consumption would have also been high.Quite a few authors tried to estimate the caloric Plant:Animal ratio (DPA) in the humans ’Paleolithic diet [2-8]. A wide variation of DPA’s was predictedwith averages ranging between 66% plants and 33% animal[4] to 35% plantsand 65% animal[2]. Alas, because in the archaeological record plants preserve poorlyor not at all, all of the estimatesrelied to a great extenton the ethnographic record of diets of recent hunter-gatherers' (HG) groups with a tacit or expressed claim for the analogybetween the periods. However, I claim that the HG's ethnographic record 1 should not be used to predict Paleolithic diets, or indeed even variability in the diet, as the ecologies of the two periods are so different as to denyany scientific validity to such prediction. Here I outline a short review of the relevant ecological conditions in support of my claim. A full paper is in preparation. Recent hunter-gatherers ethnography is a misleadingsource of Paleolithic diet reconstructionIn discussing the use ofethnographicsourced analogies in archaeology, Ascher (9)summarized his contemporaries, Clack, Willey, and Childes’ opinions thus: “...the cannon is: seek analogies in cultures which manipulates similar environments in similar ways.” In other words, the degree of similarity between the ecological and technological conditions of the known and unknown periods is the key criteria in judging the validity of ethnographic sourced analogies. A review of the recent ecological conditions revealsthat especially in one crucialaspect, availabilityand size offaunal and floral resources, there is a drastic and unbridgeablegap between the Paleolithic and the recent modern HG period. In a recent paper, Smith et al. [10] calculated the mean body weight of non-volant (not flying) terrestrial mammals during the last 2.5 million years. A drastic decline in terrestrialmammals took place from approximately 500 kgs at the beginning of the Pleistocene 2.5 million years ago to about 10kgs today. In the same vein, Bibi et al.[11] compared the faunal assemblagesof Olduvai Middle Bed II at 1.7-1.4 million years ago (Mya) to faunal communitiesin the present day Serengeti. They concluded that “The sheer diversity of species, including many large-bodied species, at Neogene and Pleistocene African sites like Olduvai, is perplexing and makes extant African faunas look depauperate in comparison.”Indeed, they present a hypothesis, supported by reduced carnivore richness in the Early Pleistocene [12], that human predation may have been the cause of the loss of largeherbivores during the Pleistocene. A significant part of the reduction occurred in the Late Pleistocene and is a global phenomenon.During the Late Quaternary Megafauna Extinction,about 90 genera of animals weighing >44 kg became extinct beginning some 50 Kya [13]. The rate of extinctionby body size follows a typical pattern in which the largest size genera became more completely extinct. In all the continents, apart from Africa and the Indian sub-continent, all genera exceeding 1000kg became completelyextinct, and those in the 1000-320 kg category became 50-100% extinct. In Africa, Some 25% of what was left in the Late Quaternary’s megafauna (>45 kg) became extinct [14].

In Africa, however, even the few large animals that remained were hardly available for hunting by HG groups that form the basis for many analogies with the Paleolithic, the Hadza, and the San. Elephants were huntedby Europeans with guns in the Hadza and San’s territories for over a hundred years. There is evidence for a drastic decline in the availability of animals as a result of herders and farmers encroachment abound [15, 16].The result is that the Hadza no longer hunt the three largest animals in Africa, elephants, rhinos, and hippos. Moreover, the disappearance of large animals, and especially elephants, caused a substantial increase in the availability of plant food sources. Elephants are known to be a formidable predator of baobab trees[17]. Baobab isthe single largest contributor of calories to the Hadza as well as a homefor theirmost popular species of honey bees.A similar phenomenon occursin the San (!Kung) territory where the mongongo tree, their staple food source, was subject to partial destruction and growth retardation when elephants were present in its vicinity [18:312]. In summary, the differences in the relative availability of plants and animals and especially big animals, between the Paleolithic and modern HG'speriod are so criticalthat they prevent any inferencefrom the recent HG DPA to Paleolithic DPA, including any conclusion regarding the degree of DPA variability during the Paleolithic. So, if ethnography and archaeologyare poor sources for DPA estimates, are there other fields of knowledge we can explore? As it turns out, physiology can be a trove of information for evolutionary DPA, as adaptations to one DPA or another are stored in our body in the forms of genetics, morphology,metabolism,andsensitivity to pathogens. Reconstruction of the Paleolithic diet based on human physiologyA more detailed reconstructionwhich was performed as a part of my Ph.D. thesis and is in preparation for publication. What follows is a short review of some of the physiological adaptations or lack thereof that provide evidence for the nature of our past diet. The first three adaptations are unique in that the authors themselves point out (maybe to their surprise) that according to their finds, we have various physiological processes that align with that of carnivores.

Weaning like a carnivore
Life history, the age at which animal reach certain stages in life like gestation, weaning, mating, and death,is strongly defined in a species. Psouni et al. [19]found that adult brain mass, limb biometrics,anddietary profile can explain 89.2% of the total variance in time to weaning. Comparing 67 species, they found humans to be in the carnivores’ group while chimpanzees and other primates with the non-carnivore's group. They conclude: "Our findings highlight the emergence of carnivory as a process fundamentally determining human evolution."Many smaller fat cellslike all carnivoresPond and Mattacks (20) compared the structure of fat cells in various types of animals. Carnivores were found to have a higher number of smaller fat cells and omnivores a smaller number of larger fat cells. Humans were found to beat the top of the carnivorous pattern. Pond and Mattacks conclude: “These figures suggest that the energy metabolism of humans is adaptedto a diet in which lipids and proteins rather than carbohydrates, make a major contribution to the energy supply.”

Stomach acidity of a unique carnivore
Beasley, Koltz (21)emphasize the role of stomach acidity in protection against pathogens. The found that carnivores’ stomachs at a pH of 2.2 are more acidic than omnivores’stomachs at a pH of 2.9 but less acidic than obligate scavengers at pH of 1.3. According to Beasley, Koltz (21) Humans had a high level of acidity of 1.5 that lies between that of obligate and facultative scavengers. Producing acidity,and retaining the stomach walls to contain that acidity,is energetically expensive, so would presumably only evolve if the level of pathogens in the human diet was high. The authors surmise that humans were more of a scavenger than we thought. However, there is a more likely conclusion if we take into account that humans were a particular kind of carnivore. Unlike other carnivores, they consumed the meat over several days either in a central place (home base) [22] or, for very large animals,where it was acquired [23]. Big animals, like elephants and bison, and even smaller animals like zebra, provide enough calories to last a 25-member HG group for days and weeks [24]. During this time the pathogen load is bound tobuildup to a higher level than even a regular scavenger encounters under normal circumstances and hence the presumed need for high acidity.

Reduced energy extraction capacity from plants.
Most plant eaters extract a large part of their energy from the fermentationof fiber by gut bacteria[25]. In primates,the fermentation takes place in the large intestine.For example, a gorillaextractssome 60% of its energyfrom fiber[26]. The fruits that chimps are consuming are also very fibrous [27].Their large intestines form 4
52% of the volume of the gut, similar to the 53% in the gorilla [28], indicating that,like a gorilla,they also drive a similarly highportion of their energy from fiber.An adaptation that preventshumans from efficientexploitation of fiber to energymay point to a shift in the dietary emphasisaway from plantstowards specialization in animal’s sourced food [See 29 considering criteria for specialization]. Our gut is 40% smaller[30], and one can therefore calculate that our large intestine, where fiber is processedto energy, is 77% smallerby volume than that of a chimpanzee our size[28]. The size and our small intestine, where -macronutrients are absorbed is 62% larger than that of a chimpanzee our size. Since the Chimpanzee was able to absorb a large amount of sugar with a shorter small intestine, The 66% extension could representan adaptation to consuming more fat and proteinin humans. Since the masticationsystem prepare the food for the gutareduced mastication system already1.7 million years ago (Mya) in H. erectussuggests that the gut size of H. erectuswas already reduced [31].We can thus propose that H. erectusspecialed in non-plant food items.The omnivorous pigs are sometimes mentionedas a good model for human nutrition [32], however,the volume of their large intestine is higher than the volume of their small intestine [32]the reserveratio in humans[28], pointing to the adaptationof pigs to highly fibrous food.The changed gut composition meets the criteria for specialization proposed by Wood and Strait (29). They propose that adaptation towards specialization is marked by a change that enables the acquisition of one resource while interrupting in the acquisition of another resource.In our case,the gut morphology adaptations both improvedanimal food exploitationand at the same time hindered the full exploitation of fibrous plant foods.Endurance running Bramble and Lieberman [33] list 22 specific adaptations to endurance running and claim they represent an adaptationto ‘persistence hunting’. There is some disagreement as to the significance of the 'persistence hunting' technique[34],butas it representsan adaptationto better mobility, it may also indicate adaptationto operating in a largerhome-range. Carnivores with a large proportion of flesh in their diets such as Canids and Felids have particularly large home-ranges whereas omnivorous carnivores like Ursidae have a narrower home-range[35].Adaptation to aspear throwingRoach et al. [36]claim that the structure of our shoulderrepresents an adaptation to carnivory. They describe howour shoulder is perfectly adaptedto throwing, which must be useful, in their opinion, mainly in hunting and protection from predators. They show that in contrast, thechimpanzee’s shoulder is adaptedto climbing trees.

This evidence may serve as another evidence for specialization in carnivory, like the smaller gut,the improved ability toobtain animal food comes at the account of reduced ability to obtain plant-sourcedfood, fruits in this case.High-fatreservesHumans have much higher fat reserves than chimps,our closest relatives [37]. Carrying a high amount of fat cost energy and reduce the speed of chasing or fleeting[38]. Most carnivores and fleeting herbivores do not pack much fatas, unlike humans, they rely on speed for predation or evasion.Recent HG were found to have enough fat reserves to fast for three weeks for men and six weeks for women[39]. This ability may represent anadaptation that is unique to carnivory of large animals by a predator who does not rely on speed. The large fat reserves may have allowed human tobridgelonger periods between less frequent hunts of largeranimalsdue to their relativelylower abundance.

The AMY1 gene -Incomplete adaptation to metabolize starch?
Humans have a varying number of AMY1 gene copies (2-12 copies [40]) which synthesize salivary amylase whereas chimpanzees have only two copies.The higher copy number may represent different degrees of adaptation to consuming starch[40] although the results of actual health markers associations with the number of copiesare equivocal [41-47].Herbivores and carnivores donotseem to have salivary amylase (although the data are limited) whereas omnivores usually produce high quantities of the enzyme [48]. This variancein the number of copies in humans in itself can be(but doesn't have to be)a testimony that the adaptationis relatively recent and have not beenfixedyet. However, until better grasp is obtainedon the timing of the change in copy number, little can be said about its significance to the question of DPA in humans.Recent genetic adaptation to tuber consumptionTubers, which are available year-round and are as energy dense as wild fruits,are mentionedas a good candidate for Paleolithic plant-based diet [49]. Populations that presently depend on tubersare enrichedin genes that are associatedwith starch metabolism, folic acid synthesis,andglycosides neutralization, but other populationsare not[50]. These adaptations presumably compensate for these tubers’ poor folic acid and relatively high contentof glycosides. The very limitedgeographicdistribution of these genes[50]maymeanthat their presence in humansis quite recentso that tubers did not form an importantpart of the human Paleolithic diet.

The earliestevidence for caries -15,000 years ago
High consumption of starch and sugars is associatedwith the development of oral cariescavities [51].Frequenciesof carious lesions in archaeological populations rangefrom 2.2–48.1% of teeth for agricultural populations, but only0–14.3% for hunter-gatherers[52]. A high prevalence of cariesfirstappearedsome 15.0 Kya in a site in Morocco, together with evidence for exploitation of starchy foods[53]. Thisrecent phenomenon may mean that high carbohydrates (plants)consumption is a relatively recentend-of-Pleistocenephenomenon.It should be pointedout that in some more recent traditional societies high starch consumption was not associated with a highprevalence of caries [54].

Paleolithic dietary reconstruction based on human Physiology –conclusion
Although physiology is only one of the sourcesfor Paleolithic dietary reconstruction, looking into the information that is storedin our bodyprovide an interesting and sometimes new evidence that we underwent substantial adaptation towards carnivory and that it started quite early in our evolution as the genus Homo. It also supports the notion thatwe remain adapted to carnivory despite over 10,000 years of agricultural subsistence. Consequently, it seems, in reply to the question at the heart of this paper,that we are adaptedto consume high quantities of protein. How high? The answer lies in reconstructing our behavior during prehistory regardingfat [24, 55].What was the protein consumption level during human evolution? The question of the desirable level of dietary protein consumption comes up in the literature and among professional and lay people who are interested in nutrition. This section tries to answer that question by discerning the Paleolithic level of consumption, assuming that it is a safelevel, following the evolutionary mismatch theory of chronic disease[56]. Protein processing for energy in humans is estimated to be physiologically limited to 35-45% of the daily calories[57, 58].If humans were at the protein limitduring the Paleolithic era, the remaining 55-65% of the calories should have come either from fat or carbohydrates, namely plants.There is ample ethnographic evidence for human dependence on and preference for animal fat as afood source. Kelly [59]writesin his authoritative book on HG: “...although ethnographic accounts abound with references to theimportance of meat they equally convey the importance of fat...”. He adds: “It, therefore,may be fatrather than protein that drives the desire for meat in many foraging societies”.

Lee [16] writes about the !Kung of the K alahari: “Fat animals are keenly desired, and all !Kungexpressa constant craving for animal fat”. The essentiality of fat is best demonstrated in Tindale’s account of the Pitjandjara of Australia[60]. He writes: "Whenkilling the animal they immediately feel the body for evidence of the presence of caul fat. If the animal is 'njuka',fatless, it is usually left unless they are themselves starving”. Coote and Shelton [61]report a similar behavioramong the Yolngu of Arnhem, Australia, saying that "Animals without fat may indeed be rejected as food".The importance of fat is also evident initsuse as a symboloffertility, sacredness, wealth, health and even life itself in recent traditional societies' rituals, linguistics and mythology [55]The archaeological record similarly showsthat many of humans’ particular acquisition and food exploitation behaviors can be interpreted as stemming from the need to obtain fat. Behaviors like the hunting of fatter animal or processing of fat from body parts at greater energetic expenditure thanwould have otherwise been needed indicate a concentration on fat as the primarycriterion in prey selectionand butchering. The preference of hunting larger animals and prime adultanimals within prey species[24, 62, 63], the preferenceto bring fatty parts to a central place and the extraction of bone grease [64],at great energetic costs,all point to a strategy of fat maximization. Thisenergetically expensive set of behaviors also supports the conclusion that plants could not provide a sufficient contribution to complement the protein at the limit of its consumption.This energetically expensive behavior is difficult to explain unless we assume that humans were at the limit of their protein consumption. Therefore, the implication for protein consumption from this reconstruction is that throughout our evolution as humans we obtaineda high portion of our calories from protein. Although no clear official statement of the upper limit on the consumption of protein has ever been published, there are reports of consumption of over 40% of the daily calories,or about 4 grams per kg body weight per day (g/kg/d) by circumpolar groups [65]. Rudman, Difulco (66)found the limit on urea removal to be 3.8 g/kg/dof protein to which the demand of structural protein at a minimum of 0.8grams per kg per day should be added [57]to a total of 4.6 g/kg/d. The present level of protein intake in the U.S.is some15.7% [67]of the daily calories. Based on consumption of 2000 calories for a 60 kgs person the currentconsumption is 314 calories whereas the Paleolithic level of consumption, according to this analysis was in the vicinity of 800 calories (40% of 2000) and possibly even higher at 1100 calories (4.6 g/kg/d X60 kgs X 4 cal/g).

Conclusion
As mentioned, this paper is just a part of a wider review, in preparation, of scientific evidence for the human evolutionary diet. Although we are undoubtedly omnivores, the biologic evidence that was presentedhere claims to show that we evolved, quite early in our evolution as the genus Homo, to becomehighly carnivorousand that we continue toretain abiologic adaptation to carnivory. This high level of carnivorymeans that during a largepart of our evolution our diet was high in protein besides being high in fat. If we look at the Paleo nutrition templateas a safety templet,this paper concludesthat it seems to be safe to consume a highportion of the diet from animal protein, possiblyto the tune of 30-40% of the daily calories. Since every calorie of protein that we do not consume is a calorie that will be consumed from another food source, the Paleo template guides us to consider the relative safety of alternatives to proteinwhen deciding on the actual level of protein consumption. Not many alternatives foods can claim to have nearly two million years of safe consumption.

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Although we are undoubtedly omnivores, we evolved quite early to become highly carnivorous and we continue to retain a biologic adaptation to carnivory