Are humans carnivores? The evolution of our place in the food web

Where do humans sit in the food chain?

Research suggests that during the Pleistocene, the human trophic level evolved to become increasingly carnivorous. This trend then reversed somewhat during the Upper Paleolithic (which ended about 11,000 years ago); this was followed by a push toward a more agricultural approach in the Neolithic period, which started 5,000 years ago.

Research also has established that by the end of the Pleistocene, there was a dramatic drop—up to 90 percent—in the average body weight of terrestrial mammals. This is best explained by hunter-gatherers hunting large mammals to extinction, such that mostly smaller ones remained [1]. Subsequent hunter-gatherer populations were, therefore, faced with a different ecology—notably, very little megafauna, a change in the types of plants available, and increased vegetation density [2].

Keep in mind that carnivores can eat things other than meat. That is, a carnivorous HTL is compatible with observations that healthy ancestral populations could live on omnivorous high-starch diets [3, 4, 5]. This could take place as long as there were enough animal-sourced foods to ensure adequate nourishment [6, 7].

Let’s take a closer look at the basis for this carnivorous HTL, according to the following parameters:

• diet quality
• fat metabolism and reserves
• genetic adaptations and starch consumption
• physiology and anatomy
• isotopes, trace elements, and dental health
• paleozoology
  

Diet quality

A high-quality human diet is calorically dense, easily digestible, and has both depth and breadth in terms of its essential macro- and micronutrient content [8]. According to these criteria, animal foods are qualitatively and quantitatively superior to plant foods.

Comparing 100 grams of plants to 100 grams of various terrestrial animals shows that in eight out of 10 key vitamins and minerals, animal foods are more nutrient dense than plants—and several times denser in most cases. Adjusting for factors like bioavailability and active nutrients makes animal foods look even more nutritious [9]. It’s well known that animal-sourced foods provide several essential micronutrients in their active forms that plants often do not.

Plant food is mainly denser in vitamin E, C, and calcium. However, the results of the two-year Bellevue “carnivore” study, as well as accounts of highly carnivorous polar societies, do not provide evidence of scurvy, vitamin E deficiency, or other such deficiencies in these populations [10]. Research has established that our bodies handle micronutrients differently, according to physiological context. When someone is on a low-carb diet, for example, more calcium is absorbed to compensate for its increased excretion, should bone resorption occur in an attempt to steady blood calcium levels [11].

Fat metabolism and reserves

Human metabolism is characterized by it’s extensive reliance on fat (both stored and from the diet) for fuel, which it can burn very efficiently [12]. This is evidenced by strong selective pressure over our evolution for the lipase enzyme – an enzyme that is critical to the storage and use of fats [13]. Likewise, comparative chromatin landscape analyses – a method used to perform extensive analysis of our chromosomes – shows a strong overall adaptation towards high-fat diets in humans and primates [14].

Humans are uniquely well adapted to ketosis, whether brought about through fasting or nutritional means [15, 16]. It’s even essential for proper brain development in infants [17]. Ketone bodies spare muscle mass in hypocaloric states [18, 19]. In ketosis, adaptive glucose sparing (i.e. physiological insulin resistance) occurs and is typical of carnivores [20]. When the genetic basis of physiological insulin was investigated by comparing Kirghiz herders from central Asia and Tajik farmers, it was found that despite eating a similar diet nowadays, the Khirgiz herders who relied more on animal foods had higher baseline adaptive glucose sparing [21].

Male and female hunter-gatherers have an average body fat level of 9 percent and 24 percent, respectively, which is quite lean by modern standards [22]. But compared to primate bonobo males and females that have less than 1 percent and less than 4 percent body fat, respectively, humans are relatively fat [23]. The fat we eat has priority storage in our subcutaneous fat tissue, even before other macronutrients do [24]. We also fit the typical carnivore pattern of adipocyte morphology, which means we have smaller and more numerous fat cells [25].

Our larger fat reserves are original to us, in the sense that they’re not a trait held by our group’s last common ancestor [26]. Our other energy source, carbohydrate, is stored in amounts (400-500 grams) about 10 times smaller than fat. Humans can earn tens of thousands of calories per hour hunting medium-sized animals, in contrast with the meager 1,431 calories from foraging plants [27]. Human specialization for hunting large animals during the Pleistocene provided even bigger returns [28]. Our fat stores and our hunting seem to go hand in hand.

Genetic adaptations and starch consumption

The evidence that points to an accumulated genetic adaptation to tuber consumption is rather recent on our evolutionary timescale [29]. It suggests tubers weren’t a big part of our diet previously [30]. The human AMY1 gene is expressed in many of our organs for the breakdown of starch and glycogen. Several studies have hypothesized that people with a low number of AMY1 copies would suffer from higher rates of obesity and diabetes on a high-starch diet. However, the evidence doesn’t support that [31, 32].

The APOE4 gene is involved in the metabolism of fat and cholesterol in addition to LDL receptor interactions. It underwent strong selective pressure as evidenced by 15 percent of the world’s population having it today and up to 40-50 percent in certain populations [33]. When eating a highly carnivorous diet—which could have a higher pathogen burden—APOE4 may help us retain cognitive functions [34].

Physiology and anatomy

The stomach of a carnivore has a pH of 2.2, an omnivore 2.9, and a scavenger 1.3. Humans have a stomach acid pH of 1.5, placing us more towards the high end of the carnivory spectrum between obligate and facultative scavengers in that regard. This may explain why hunting populations can process much of their animal food by drying and fermenting it, as well as putrefying the meat and fat without harm [35].

Relative to chimpanzee body size, the human colon is 77 percent smaller and the intestine 64 percent longer [36, 37]. The smaller our colons, the less fiber we can ferment into usable energy, which means the less we can rely upon fibrous plant foods to meet our daily caloric needs. Body size is related to trophic level, and Homo’s enlarging body is linked to carnivory [38].

Carnivore behaviors

Hunter-gatherer populations are known to abandon prey when they’re too lean [39]. Instead, they’ll target animals that appear fatter [40], especially large adults [41]. Adaptations increasing endurance, especially in hot environments, enabled our ancestors to add “persistence hunting” to their skill set and broadened hunting territories [42]. In one paper, researchers correctly predicted multiple behaviors evolving in humans relating to increased predation [43].

Humans have an early weaning age (less than three years old) relative to other species, which is strongly associated with carnivory level. Some authors “highlight the emergence of carnivory as a process fundamentally determining human evolution” [44]. Male and female modern Hadza hunter-gatherers reach peak food-acquisition productivity from age 40 onwards [45], suggesting a selection for “experience” that resulted in longevity [46]. Animal foods are more time/calorie efficient than plants, and thus advantageous [47].

We also evolved the ability to throw weapons at prey, which gave us a crucial edge to become apex predators [48]. Anthropologists have argued that carnivory was crucial for our survival of the extremely cold Eurasian winter [49]. During the Upper Paleolithic, wolves were domesticated, thus extending our hunting-abilities, which would in turn reinforce our carnivory [50].

Isotopes, trace elements, and dental health

Stable isotope studies suggest European hunter-gatherers mostly ate a carnivorous diet during the Upper Paleolithic, placing them at or above the trophic level of wolves [51]. Using a modified trace elements method on tooth samples, early Homo was found to be indistinguishable from carnivores [52].

Although tooth plaque isn’t suitable for determining the HTL within the vast zooarchaeological landscape [53, 54], it may be marginally accurate for identifying shifts. For instance, Neanderthals were known to rely heavily on animal-sourced foods and only showed six caries (signs of decay) out of 1,250 of their teeth that were examined [55]. Caries started appearing in substantial numbers between 13,700 and 15,000 years ago in Morocco, alongside evidence of increased starch consumption [56]. The low occurrence of caries during most of the Pleistocene corresponds to a low carbohydrate, high HTL pattern.

Paleozoology

Across species, carnivore size dictates prey size. The majority of present-day predators over 15-20 kilograms focus on hunting animals under half their size, in order to benefit from the bioenergetic perspective [57]. It follows that paleolithic humans, who were relatively large carnivores, didn’t derive large amounts of nutrition from insects, unlike what is argued by Lesnik [58].

Hunting large prey as humans did is exclusively associated with hypercarnivory [59]. It is likely that humans preferred large herbivores given the abundance of their biomass, the relative ease of hunting them, net caloric returns, and their higher fat content, which accommodates physiological limits on protein consumption [60].

Conclusion

It’s difficult to consider that humans are anything other than omnivores, given our spectacular range of diets, and our mastery of technologies that have enabled us to further expand our already vast dietary repertoire. Nevertheless, the evidence above suggests that humans evolved as carnivores. A combination of technology and physiology enabled a wide range of plants to be included on top of that essential carnivorous base.

References

[1] Smith, Felisa A., et al. “The Accelerating Influence of Humans on Mammalian Macroecological Patterns over the Late Quaternary.” Quaternary Science Reviews, vol. 211, 2019, pp. 1–16., doi:10.1016/j.quascirev.2019.02.031.

[2] Doughty, C. E., Wolf, A., and Field, C. B. (2010), Biophysical feedbacks between the Pleistocene megafauna extinction and climate: The first human‐induced global warming? Geophys. Res. Lett., 37, L15703, doi:10.1029/2010GL043985.

[3] Prior, I A et al. “Cholesterol, coconuts, and diet on Polynesian atolls: a natural experiment: the Pukapuka and Tokelau island studies.” The American journal of clinical nutrition vol. 34,8 (1981): 1552-61. doi:10.1093/ajcn/34.8.1552

[4] Lindeberg, S et al. “Low serum insulin in traditional Pacific Islanders--the Kitava Study.” Metabolism: clinical and experimental vol. 48,10 (1999): 1216-9. doi:10.1016/s0026-0495(99)90258-5

[5] Price, Weston A. Nutrition and Physical Degeneration: a Comparison of Primitive and Modern Diets and Their Effects. Lightning Source, 2010, pdfs.semanticscholar.org/eb03/439a9543410a8a45d24d3b82de7e6b9e3d67.pdf.

[6] O'Hearn, Amber. “Can a carnivore diet provide all essential nutrients?.” Current opinion in endocrinology, diabetes, and obesity vol. 27,5 (2020): 312-316. doi:10.1097/MED.0000000000000576

[7] Protein and Amino Acid Requirements in Human Nutrition. World Health Organization, 2007.

[8] &Na; “Editorial Introductions.” Current Opinion in Endocrinology & Diabetes, vol. 13, no. 1, 2006, doi:10.1097/01.med.0000202322.48380.36.

[9] Frossard, E., Bucher, M., Mächler, F., Mozafar, A. and Hurrell, R. (2000), Potential for increasing the content and bioavailability of Fe, Zn and Ca in plants for human nutrition. J. Sci. Food Agric., 80: 861-879. doi:10.1002/(SICI)1097-0010(20000515)80:7<861::AID-JSFA601>3.0.CO;2-P

[10] McClellan, Walter S, and Eugene F Du Bois. “Clinical Calorimetry: XLV. Prolonged Meat Diets with a Study of Kidney Function and Ketosis.” The Journal of Biological Chemistry, 1930, doi:https://www.jbc.org/.

[11] Cao, Jay J et al. “A diet high in meat protein and potential renal acid load increases fractional calcium absorption and urinary calcium excretion without affecting markers of bone resorption or formation in postmenopausal women.” The Journal of nutrition vol. 141,3 (2011): 391-7. doi:10.3945/jn.110.129361

[12] Mattson, Mark P et al. “Intermittent metabolic switching, neuroplasticity and brain health.” Nature reviews. Neuroscience vol. 19,2 (2018): 63-80. doi:10.1038/nrn.2017.156

[13] Vining, Alexander Q, and Charles L Nunn. “Evolutionary change in physiological phenotypes along the human lineage.” Evolution, medicine, and public health vol. 2016,1 312-324. 2 Oct. 2016, doi:10.1093/emph/eow026

[14] Swain-Lenz, Devjanee et al. “Comparative Analyses of Chromatin Landscape in White Adipose Tissue Suggest Humans May Have Less Beigeing Potential than Other Primates.” Genome biology and evolution vol. 11,7 (2019): 1997-2008. doi:10.1093/gbe/evz134

[15] Cahill, G F Jr, and O E Owen. “Starvation and survival.” Transactions of the American Clinical and Climatological Association vol. 79 (1968): 13-20.

[16] Dashti, Hussein M et al. “Long-term effects of a ketogenic diet in obese patients.” Experimental and clinical cardiology vol. 9,3 (2004): 200-5.

[17] Cunnane, Stephen C. “L'évolution du cerveau humain : de la matière grasse à la matière grise” [Survival of the fattest: the key to human brain evolution]. Medecine sciences : M/S vol. 22,6-7 (2006): 659-63. doi:10.1051/medsci/20062267659

[18] Manninen, Anssi H. “Very-low-carbohydrate diets and preservation of muscle mass.” Nutrition & metabolism vol. 3 9. 31 Jan. 2006, doi:10.1186/1743-7075-3-9

[19] “How Ketones Spare Protein In Starvation.”Nutrition Reviews, vol. 47, no. 3, 1 Mar. 1989, pp. 80–81., doi:10.1111/j.1753-4887.1989.tb02798.x.

[20] Colagiuri, S, and J Brand Miller. “The 'carnivore connection'--evolutionary aspects of insulin resistance.” European journal of clinical nutrition vol. 56 Suppl 1 (2002): S30-5. doi:10.1038/sj.ejcn.1601351

[21] Ségurel, Laure, et al. “Positive Selection of Protective Variants for Type 2 Diabetes from the Neolithic Onward: a Case Study in Central Asia.” European Journal of Human Genetics, vol. 21, 2013, pp. 1146–1151., doi:10.1038/ejhg.2012.295.

[22] Pontzer, H., Wood, B. M., and Raichlen, D. A. (2018) "Hunter‐gatherers as models in public health." Obesity Reviews, 19: 24– 35. https://doi.org/10.1111/obr.12785.

[23] Zihlman, Adrienne L, and Debra R Bolter. “Body composition in Pan paniscus compared with Homo sapiens has implications for changes during human evolution.” Proceedings of the National Academy of Sciences of the United States of America vol. 112,24 (2015): 7466-71. doi:10.1073/pnas.1505071112

[24] Frayn, K N. “Adipose tissue as a buffer for daily lipid flux.” Diabetologia vol. 45,9 (2002): 1201-10. doi:10.1007/s00125-002-0873-y

[25] Pond, Caroline M, and Christine A Mattacks. “Body mass and natural diet as determinants of the number and volume of adipocytes in eutherian mammals.” Journal of morphology vol. 185,2 (1985): 183-193. doi:10.1002/jmor.1051850204

[26] Pontzer, Herman. “Energy Expenditure in Humans and Other Primates: A New Synthesis.” Annual Review of Anthropology, vol. 44, no. 1, 2015, pp. 169–187., doi:10.1146/annurev-anthro-102214-013925.

[27] Kelly, Robert L. The Lifeways of Hunter-Gatherers: The Foraging Spectrum. Cambridge University Press, 2013.

[28] Lemke, Ashley K. Foraging in the Past: Archaeological Studies of Hunter-Gatherer Diversity. University Press of Colorado., 2018.

[29] Hancock, A. M., et al. “Human Adaptations to Diet, Subsistence, and Ecoregion Are Due to Subtle Shifts in Allele Frequency.” Proceedings of the National Academy of Sciences, vol. 107, no. Supplement_2, 2010, pp. 8924–8930., doi:10.1073/pnas.0914625107.

[30] Wrangham, Richard W, et al. “The Raw and the Stolen: Cooking and the Ecology of Human Origins.” Current Anthropology, vol. 40, no. 5, 2000, p. 567., doi:10.2307/3596391.

[31] Usher, Christina L et al. “Structural forms of the human amylase locus and their relationships to SNPs, haplotypes and obesity.” Nature genetics vol. 47,8 (2015): 921-5. doi:10.1038/ng.3340

[32] Fernández, Catalina I., and Andrea S. Wiley. “Rethinking the Starch Digestion Hypothesis forAMY1copy Number Variation in Humans.” American Journal of Physical Anthropology, vol. 163, no. 4, 2017, pp. 645–657., doi:10.1002/ajpa.23237.

[33] Eisenberg, Dan T A et al. “Worldwide allele frequencies of the human apolipoprotein E gene: climate, local adaptations, and evolutionary history.” American journal of physical anthropology vol. 143,1 (2010): 100-11. doi:10.1002/ajpa.21298

[34] Trumble, Benjamin C., et al. “Apolipoprotein E4 Is Associated with Improved Cognitive Function in Amazonian Forager‐Horticulturalists with a High Parasite Burden.” The FASEB Journal, vol. 31, no. 4, 2016, pp. 1508–1515., doi:10.1096/fj.201601084r.

[35] Speth, John D. “Putrid Meat and Fish in the Eurasian Middle and Upper Paleolithic: Are We Missing a Key Part of Neanderthal and Modern Human Diet?” PaleoAnthropology Society, 2017, doi:http://www.paleoanthro.org/med....

[36] Aiello, Leslie C., and Peter Wheeler. “The Expensive-Tissue Hypothesis: The Brain and the Digestive System in Human and Primate Evolution.” Current Anthropology, vol. 36, no. 2, 1995, pp. 199–221. JSTOR, www.jstor.org/stable/2744104. Accessed 6 Oct. 2020.

[37] Milton, Katharine. “Milton, Katharine. (2009). Primate Diets and Gut Morphology: Implications for Hominid Evolution. Food and Evolution: Toward a Theory of Human Food Habits. 93-115. .” Research Gate, pp. 93–115., www.researchgate.net/publication/281674127_Primate_diets_and_gut_morphology_Implications_for_hominid_evolution/citation/download.

[38] Churchill, Steven Emilio, et al. “Home-Range Size in Large-Bodied Carnivores as a Model for Predicting Neandertal Territory Size.” Evolutionary Anthropology: Issues, News, and Reviews, vol. 25, no. 3, 2016, pp. 117–123., doi:10.1002/evan.21483.

[39] Forrest, John. “Jeremy Coote and Anthony Shelton, Eds. Anthropology, Art, and Aesthetics.:Anthropology, Art, and Aesthetics.” Museum Anthropology, vol. 19, no. 1, 1995, pp. 67–68., doi:10.1525/mua.1995.19.1.67.

[40] Brink, Jack W. Imagining Head Smashed In Aboriginal Buffalo Hunting on the Northern Plains. Athabasca University Press, 2008, justmeat.co/docs/imagining-head-smashed-in-jack-w-brink.pdf.

[41] Bunn, Henry T., and Alia N. Gurtov. “Prey Mortality Profiles Indicate That Early Pleistocene Homo at Olduvai Was an Ambush Predator.” Quaternary International, vol. 322-323, 2014, pp. 44–53., doi:10.1016/j.quaint.2013.11.002.

[42] Hora, Martin et al. “Dehydration and persistence hunting in Homo erectus.” Journal of human evolution vol. 138 (2020): 102682. doi:10.1016/j.jhevol.2019.102682

[43] Shipman, Pat, and Alan Walker. “The Costs of Becoming a Predator.” Journal of Human Evolution, vol. 18, no. 4, 1989, pp. 373–392., doi:10.1016/0047-2484(89)90037-7.

[44] Psouni, Elia, et al. “Impact of Carnivory on Human Development and Evolution Revealed by a New Unifying Model of Weaning in Mammals.” PLoS ONE, vol. 7, no. 4, 2012, doi:10.1371/journal.pone.0032452.

[45] Marlowe, Frank W. The Hadza: Hunter-Gatherers of Tanzania. 1st ed., University of California Press, 2010, www.jstor.org/stable/10.1525/j.ctt1pp17z, Accessed 6 Oct. 2020.

[46] Kaplan, Hillard, et al. “A Theory of Human Life History Evolution: Diet, Intelligence, and Longevity.” Evolutionary Anthropology: Issues, News, and Reviews, vol. 9, no. 4, 2000, pp. 156–185., doi:10.1002/1520-6505(2000)9:4<156::aid-evan5>3.0.co;2-7.

[47] Kuhn, Steven L, et al. “The Early Upper Paleolithic Occupations at Üçağızlı Cave (Hatay, Turkey).” Journal of Human Evolution, vol. 56, no. 2, Feb. 2009, pp. 87–113., doi:https://doi.org/10.1016/j.jhev....

[48] Roach, Neil T., and Brian G. Richmond. “Clavicle Length, Throwing Performance and the Reconstruction of the Homo Erectus Shoulder.” Journal of Human Evolution, vol. 80, 2015, pp. 107–113., doi:10.1016/j.jhevol.2014.09.004.

[49] Stiner, Mary C. “Carnivory, Coevolution, and the Geographic Spread of the Genus Homo.” Journal of Archaeological Research, vol. 10, 2002, pp. 1–63., doi:https://doi.org/10.1023/A:1014....

[50] Camarós, Edgard, et al. “The Evolution of Paleolithic Hominin–Carnivore Interaction Written in Teeth: Stories from the Swabian Jura (Germany).” Journal of Archaeological Science: Reports, vol. 6, 2016, pp. 798–809., doi:10.1016/j.jasrep.2015.11.010.

[51] Richards, M. P., and E. Trinkaus. “Isotopic Evidence for the Diets of European Neanderthals and Early Modern Humans.” Proceedings of the National Academy of Sciences, vol. 106, no. 38, 2009, pp. 16034–16039., doi:10.1073/pnas.0903821106.

[52] Balter, Vincent et al. “Evidence for dietary change but not landscape use in South African early hominins.” Nature vol. 489,7417 (2012): 558-60. doi:10.1038/nature11349

[53] Casteren, Adam Van, et al. “Hard Plant Tissues Do Not Contribute Meaningfully to Dental Microwear: Evolutionary Implications.” Scientific Reports, vol. 10, no. 1, 2020, doi:10.1038/s41598-019-57403-w.

[54] Pérez-Pérez, Alejandro et al. “Non-occlusal dental microwear variability in a sample of Middle and Late Pleistocene human populations from Europe and the Near East.” Journal of human evolution vol. 44,4 (2003): 497-513. doi:10.1016/s0047-2484(03)00030-7

[55] “An Anthropological Overview.” Caries Through Time: An Anthropological Overview, by Luis Pezo Lanfranco and Sabine Eggers, INTECH Open Access Publisher, 2012, pp. 3–34.

[56] Humphrey, L. T., et al. “Earliest Evidence for Caries and Exploitation of Starchy Plant Foods in Pleistocene Hunter-Gatherers from Morocco.” Proceedings of the National Academy of Sciences, vol. 111, no. 3, 2014, pp. 954–959., doi:10.1073/pnas.1318176111.

[57] Meachen-Samuels, Julie, and Blaire Van Valkenburgh. “Craniodental Indicators of Prey Size Preference in the Felidae.” Biological Journal of the Linnean Society, vol. 96, no. 4, 2009, pp. 784–799., doi:10.1111/j.1095-8312.2008.01169.x.

[58] Lesnik, Julie J. Edible Insects and Human Evolution. University Press of Florida, 2019.

[59] Oksanen, Lauri. “Faculty Opinions Recommendation of The Impact of Large Terrestrial Carnivores on Pleistocene Ecosystems.” Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature, 2016, doi:10.3410/f.725882781.793519459.

[60] Ben-Dor, Miki, et al. “Man the Fat Hunter: The Demise of Homo Erectus and the Emergence of a New Hominin Lineage in the Middle Pleistocene (Ca. 400 Kyr) Levant.” PLoS ONE, vol. 6, no. 12, 2011, doi:10.1371/journal.pone.0028689.