The evolution of the human trophic level during the Pleistocene. Miki Ben‐Dor Raphael Sirtoli Ran Barkai. American Journal of Physical Anthropology, March 5 2021. https://doi.org/10.1002/ajpa.24247
Abstract: The human trophic level (HTL) during the Pleistocene and its degree of variability serve, explicitly or tacitly, as the basis of many explanations for human evolution, behavior, and culture. Previous attempts to reconstruct the HTL have relied heavily on an analogy with recent hunter‐gatherer groups' diets. In addition to technological differences, recent findings of substantial ecological differences between the Pleistocene and the Anthropocene cast doubt regarding that analogy's validity. Surprisingly little systematic evolution‐guided evidence served to reconstruct HTL. Here, we reconstruct the HTL during the Pleistocene by reviewing evidence for the impact of the HTL on the biological, ecological, and behavioral systems derived from various existing studies. We adapt a paleobiological and paleoecological approach, including evidence from human physiology and genetics, archaeology, paleontology, and zoology, and identified 25 sources of evidence in total. The evidence shows that the trophic level of the Homo lineage that most probably led to modern humans evolved from a low base to a high, carnivorous position during the Pleistocene, beginning with Homo habilis and peaking in Homo erectus. A reversal of that trend appears in the Upper Paleolithic, strengthening in the Mesolithic/Epipaleolithic and Neolithic, and culminating with the advent of agriculture. We conclude that it is possible to reach a credible reconstruction of the HTL without relying on a simple analogy with recent hunter‐gatherers' diets. The memory of an adaptation to a trophic level that is embedded in modern humans' biology in the form of genetics, metabolism, and morphology is a fruitful line of investigation of past HTLs, whose potential we have only started to explore.
7 DISCUSSION
7.1 Summary of the evidence
The actual HTL during the Pleistocene is unobservable; therefore, we looked for evidence of the impact of the HTL on the studied humans' biological, behavioral, and ecological systems. Observing only its reflection and not the HTL itself, we are left employing varying degrees of interpretation in forming an opinion about what HTL caused a specific impact and whether it denotes a step toward specialization or generalization. We reviewed 25 different evidence sources, 15 of which are biological and the remainder archaeological, paleontological, zoological, and ethnographic. With a list of 25 evidence items, by necessity, the descriptions of the findings and the justification of the various interpretations cannot be thorough, leaving much room for further review and debate. One of the main aims of this article was to present the power of paleobiology in particular and to cast a wide net of scientific fields in general in investigating HTL. The evidence here is by no means comprehensive. There is additional genetic and physiological evidence for biological adaptations to a higher and lower trophic level in the past and additional evidence for Paleolithic HTLs in other fields of science, which we chose not to include, and others that we probably missed. Thus, although we do not shy away from presenting a clear hypothesis based on the evidence, the article should be looked at as a first iteration in what hopefully will be a continuous scientific endeavor.
The presented evidence can be organized into three epistemological groups with potentially increasing levels of validity regarding a specific trophic level (see text or Table 2 for a description of the evidence):
| Item | Description |
|---|---|
| Biology | |
| Bioenergetics | Humans had high energetic requirements for a given body mass and had a shorter time during the day to acquire and consume food. Hunting provides tenfold higher energetic return per hour compared to plants, leaving little room for flexibility (plasticity) between the two dietary components. Animals tend to specialize in the highest return items in their niche. (Specialization) |
| Diet quality | In primates, a larger brain is associated with high energy density food. With the largest brain among primates, humans are likely to have targeted the highest density food, animal fats, and proteins. Brain size declined during the terminal Pleistocene, and subsequent Holocene. Diet quality declined at the same time with the increased consumption of plants. (Specialization) |
| Higher fat reserves | With much higher body fat reserves than primates, humans are uniquely adapted to lengthy fasting. This adaptation may have helped with overcoming the erratic encountering of large prey. (Change in trophic level) (Change in trophic level) |
| Genetic and metabolic adaptation to a high‐fat diet | Humans adapted to higher fat diets, presumably from animals. Study (Swain‐Lenz et al., 2019): “suggests that humans shut down regions of the genome to accommodate a high‐fat diet while chimpanzees open regions of the genome to accommodate a high sugar diet” (Change in trophic level) |
| FADS‐Omega3 oils metabolism | Genetic changes in the FADS gene in African humans 85 Kya allowed for a slight increase in the conversion of the plant DHA precursor to DHA signaling adaptation to a higher plant diet (Change in trophic level) |
| Late adaptations to tubers' consumption | Tubers were assumed to be a mainstay of Paleolithic diets that cooking could prepare for consumption. Recent groups that consume high quantities of tubers have specific genetic adaptations to deal with toxins and antinutrients in tubers. Other humans are not well adapted to consume large quantities of tubers. (Change in trophic level) |
| Stomach acidity | Higher stomach acidity is found in carnivores to fight meat‐borne pathogens. Humans' stomach acidity is even higher than in carnivores, equaling that of scavengers. Adaptation may have evolved to allow large animals' consumption in a central place over days and weeks with pathogen build‐up. (Categorization to a trophic group) |
| Insulin resistance | Humans, like carnivores, have a low physiological (non‐pathological) insulin sensitivity. |
| Gut morphology | Humans' gut morphology and relative size are radically different from chimpanzees' gut. Longer small intestines and shorter large intestines are typical of carnivores' gut morphology and limit humans' ability to extract energy from plants' fiber. (Specialization) |
| Mastication | Reduction of the masticatory system size already in Homo erectus, compared to early hominins, who relied on terrestrial vegetation as a food source. The reduced size is compatible with meat and fat consumption. (Aiello & Wheeler, 1995; Zink & Lieberman, 2016) (Change in trophic level) |
| Cooking | Cooking was hypothesized to have enabled plants' high consumption despite the need for a high‐quality diet, starting with H. erectus. Other researchers argue that habitual use of fire is evident only around 0.4 Mya. Also, a fire has other uses and is costly to maintain. (Change in trophic level) |
| Postcranial morphology | A set of adaptations for endurance running is found already in H. erectus, useful in hunting. Shoulders adapted to spear‐throwing in H. erectus. But limited tree climbing capability. (Specialization) |
| Adipocyte morphology | Similar to the morphology in carnivores. “These figures suggest that the energy metabolism of humans is adapted to a diet in which lipids and proteins rather than carbohydrates, make a major contribution to the energy supply.” (Pond & Mattacks, 1985). (Categorization to a trophic group) |
| Age at weaning | Carnivores wean at a younger age, as do humans. Early weaning “highlight the emergence of carnivory as a process fundamentally determining human evolution” (Psouni et al., 2012). (Categorization to a trophic group) |
| Longevity | Kaplan et al. (2007) hypothesized that a large part of the group depended on experienced hunters due to long childhood. Extended longevity in humans evolved to allow utilization of hunting proficiency, which peaks by age 40. The grandmother hypothesis claim women's longevity allowed additional gathering. (Change in trophic level) |
| Vitamins | Hypothesis for required nutritional diversity to supply vitamins is contested. It appears that all vitamins, including vitamin C are supplied in adequate quantities on a carnivorous diet. (Neutral) |
| Multicopy AMY1 genes | Multi‐copies of the AMY1 gene have been hypothesized as adaptive to high starch diets. However, both findings of its possible lack of functionality and the unclear timing of its appearance limits the use of the evidence to support a change in trophic level. (Change in trophic level) |
| Archaeology | |
| Plants | Plants were consumed throughout the Paleolithic, but their relative dietary contribution is difficult to assess. Recent advances in plant residues identification in dental pluck provide non‐quantitative evidence of widespread plants' consumption. Division of labor may point to a background level of plant supply, but the evidence is based largely on ethnography, which may not be analogous to the Pleistocene. (Inconclusive) |
| Stone tools | Stone tools specific to plant food utilization appear only some 40 Kya, and their prevalence increases just before the appearance of agriculture, signaling increased plant consumption toward the end of the Paleolithic. (Change in trophic level) |
| Zooarchaeology | First access to large prey, denoting hunting, appears already in H. erectus archaeological sites 1.5 Mya. Humans also hunted large carnivores. (Change in trophic level) |
| Targeting fat | Humans concentrated on hunting fatty animals at substantial energetic costs. They preferentially brought fatty parts to base camps, hunted fattier prime adults, and exploited bone fat. That behavior may indicate that plants could not have been easily obtained to complete constrained protein consumption. (Specialization) |
| Stable Isotopes | Nitrogen 15N isotope measurement of human fossil collagen residues is the most extensively used method for determining trophic level in the last 50 thousand years. All studies show that humans were highly carnivorous until very late, before the appearance of agriculture. The method has some shortcomings but was able to identify variation in trophic level among present‐day traditional groups. (Categorization to a trophic group) |
| Dental pathology | Dental caries, evidence of substantial consumption of carbohydrates, appeared only some 15 Kya in groups with evidence of high plant food consumption. (Change in trophic level) |
| Dental wear | Different wear on fossilized teeth as a result of different diets has the potential to reconstruct diets. However, the claim for the reconstruction of variable diets in Paleolithic humans could not be verified as the comparison the groups' diets were unclear. (Inconclusive) |
| Behavioral adaptations | A comparison of humans' behavior patterns with chimpanzees and social carnivores found that humans have carnivore‐like behavior patterns. Food sharing, alloparenting, labor division, and social flexibility are among the shared carnivorous behaviors. (Categorization to a trophic group) |
| Others | |
| Paleontological evidence | Evidence for hunting by H. erectus 1.5 Mya was associated with the extinction of several large carnivores, but not smaller carnivores. This suggests that H. erectus became a member of the large carnivores' guild. Extinction of large carnivores in Europe also coincided with the arrival of humans (Categorization to a trophic group) Extinctions of large herbivores were associated with humans' presence in Africa and arrival to continents and islands, such as Australia and America, suggesting preferential hunting of large prey. |
| Zoological analogy | Humans were predators of large prey. In carnivores, predation on large prey is exclusively associated with hypercarnivory, i.e., consuming over 70% of the diet from animals. (Categorization to a trophic group) |
| Ethnography | Variability in trophic level in the ethnographic context is frequently mentioned as proof of HTL variability during the Paleolithic. However, ecological and technological considerations limit the analogy to the terminal Paleolithic. (Change in trophic level) |
7.2 Type 1. Change in trophic level
This group includes evidence for physiological or behavioral adaptations to acquire and consume higher or lower amounts of either animal or plant‐sourced food. There is no argument that the evolution of the genus Homo was associated with increasing HTLs in H. habilis and further in H. erectus; therefore, it is not surprising that most of this type of evidence in the Lower Paleolithic includes evidence for adaptation to carnivory. Detailing these pieces of evidence may thus appear to be superfluous; however, identifying a trend in the number and timing of the acquisition of the adaptation may supply important indications for the occurrence of a change in trophic level. Accumulation of type 1 evidence in the Late UP supports a significant change to lower HTL at that period. Also, evidence in one period and not in the other can be interpreted as evidence for a different HTL in the last. For example, if we accept that the appearance of the AMY 1 gene multicopy sometime in H. sapiens evolution suggests a higher consumption of starch, we have to accept that there was no pressure to adapt in prior species to high consumption of starch. The same logic applies to the appearance of grains handling stone tools and dental pathology that appear only toward the Paleolithic end.
7.3 Type 2. Specialization—Reduced flexibility
Since we cannot observe our subjects, evidence for specialization is defined here as evidence that is similar to Type 1 but that, at the same time, potentially reducing the phenotypic plasticity of humans by hindering the acquisition or assimilation of the other food group (plant or animal).
Specialization and generalization must be defined with reference to particular axes such as temperature, habitat, and feeding (Futuyma & Moreno, 1988). Pineda‐Munoz and Alroy (2014) defined feeding specialization as selecting 50% or more of the food from a certain food group (fruits, seeds, green plants, insects, or vertebrates). By this definition, humans could be called specialists if they selected to consume 50% or more of their diet from vertebrates or another group of plants or invertebrates.
Another axis on which specialization can be defined is prey size. Large carnivores specialize in large prey. Evidence for humans' specialization in large herbivores can contribute to the continuing debate regarding humans' role in megafauna extinction (Faith et al., 2020; Faurby et al., 2020; Sandom et al., 2014; F. A. Smith et al., 2018; Werdelin & Lewis, 2013) and the implications of megafauna extinction on humans. Potts et al. (2018) identified an association between prey size decline during the Middle Pleistocene and the appearance of the MSA, and Ben‐Dor et al. (2011) further proposed that the extinction of elephants in the Southern Levant led to the appearance of the Acheulo‐Yabrudian cultural complex 420 Kya. Ben‐Dor and Barkai (2020a) have argued that humans preferred to acquire large prey and that large prey is underrepresented in zooarchaeological assemblages (Ben‐Dor & Barkai, 2020b). Listed in Table 3 is evidence, among the ones collected here, that can be interpreted as supporting humans' specialization in acquiring large prey.
| Bioenergetic | Large prey provides higher energetic returns than smaller prey. The need to substitute large prey for smaller prey is energetically costly. |
| Higher fat reserves | Large prey is less abundant than smaller prey. Fat reserves may have evolved to allow extended fasting of several weeks, thereby bridging an erratic encountering rate with large prey. Humans have adapted to easily synthesize ketones to replace glucose as an energy source for the brain. |
| Stomach acidity | Stronger acidity than carnivores' can be interpreted as an adaptation to a large prey's protracted consumption over days and weeks, whereby humans are acting as scavengers of their prey. |
| Targeting fat | The recognition of targeting fat as a driver of human behavior supports the importance of large, higher fat bearing animals to humans' survival. |
| Stable isotopes | Higher levels of nitrogen isotope 15 than carnivores were interpreted by researchers as testifying to the higher consumption of large prey than other carnivores. |
| Paleontology | A decline in the guild of large prey carnivores 1.5 Mya is interpreted as resulting from humans' entrance to the guild. Also, the extinction of large prey throughout the Pleistocene is interpreted by some researchers as anthropogenic, testifying to humans' preference for large prey. |
| Zoological analogy | Large social carnivores hunt large prey. |
| Ethnography | Interpreting ethnographic and Upper Paleolithic technologies as an adaptation to the acquisition of smaller prey means that humans were less adapted to the acquisition of smaller prey in earlier periods. |
Dietary plasticity is a function of phenotypic plasticity (Fox et al., 2019) and technological and ecological factors. In many cases, evolution is a process of solving problems with trade‐offs (Garland, 2014). Identifying features that were traded‐off in specific adaptations could inform us of changing dietary phenotypic plasticity levels. Relative energetic returns on primary (plant) and secondary (animal) producers are key to assessing plasticity's ecological potential. In humans, technology can expend plasticity by enabling and increasing the energetic return on the acquisition of certain food items. Bows for the hunting of smaller, faster prey and grinding stones are two examples of such technologies.
We mainly listed specialization adaptations that affected phenotypic plasticity, but there are technological and ecological pieces of evidence that potentially changed dietary plasticity like the invention of bows that increased the level of plasticity regarding prey size and the appearance and disappearance of savannas with the accompanied change in primary to secondary production ratios that swayed plasticity toward primary or secondary producers.
7.4 Type 3. Categorization to a trophic group
All the eight pieces of evidence of membership in a trophic group concluded that humans were carnivores. Assigning humans to a specific dietary trophic group has the highest potential validity, as it answers the research question with minimal interpretation.
In some cases, interpretation is required to assign a phenomenon to HTL. Belonging to the carnivores' trophic groups still does not tell us if humans were 90% or 50% carnivores. It does tell us, however, that humans were carnivorous enough and carnivorous long enough to justify physiological and behavioral adaptations unique to carnivores. Following the zoological analogy with large social carnivores that acquire large prey, we hypothesized that humans were hypercarnivores, defined as consuming more than 70% of the diet from animal sources.
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