Evolutionary basis for the human diet: consequences for human health
P. Andrews, R.J. Johnson
First published: 16 November 2019 https://doi.org/10.1111/joim.13011Citations: 22
Content List – This is an article from the symposium: “Bioinspirational medicine”.
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Abstract
The relationship of evolution with diet and environment can provide insights into modern disease. Fossil evidence shows apes, and early human ancestors were fruit eaters living in environments with strongly seasonal climates. Rapid cooling at the end of the Middle Miocene (15–12 Ma: millions of years ago) increased seasonality in Africa and Europe, and ape survival may be linked with a mutation in uric acid metabolism. Climate stabilized in the later Miocene and Pliocene (12–5 Ma), and fossil apes and early hominins were both adapted for life on ground and in trees. Around 2.5 Ma, early species of Homo introduced more animal products into their diet, and this coincided with developing bipedalism, stone tool technology and increase in brain size. Early species of Homo such as Homo habilis still lived in woodland habitats, and the major habitat shift in human evolution occurred at 1.8 Ma with the origin of Homo erectus. Homo erectus had increased body size, greater hunting skills, a diet rich in meat, control of fire and understanding about cooking food, and moved from woodland to savannah. Group size may also have increased at the same time, facilitating the transmission of knowledge from one generation to the next. The earliest fossils of Homo sapiens appeared about 300 kyr, but they had separated from Neanderthals by 480 kyr or earlier. Their diet shifted towards grain-based foods about 100 kyr ago, and settled agriculture developed about 10 kyr ago. This pattern remains for many populations to this day and provides important insights into current burden of lifestyle diseases.

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Content List – This is an article from the symposium: “Bioinspirational medicine”.

Introduction
Human evolution is strongly influenced by changes in the environment and diet. Our basic tenet is that understanding of modern diseases can be aided by insights from the past, and that knowledge of evolutionary processes and our interactions with the environment may provide insights into the challenges we face as a species as we progress through changing environments that we are, in part, driving. The approach we will take to understand human dietary evolution will be to evaluate environment and diet as they relate in time from fossil apes to modern humans.

The evolution of humans from ancestral apes, to hominins (members of the human lineage) to modern Homo sapiens can be evaluated in part by evaluating the fossil record as it relates to changes in the environment and diet. Fruit is the primary diet of apes and early hominins, and as it is dispersed in space and time, this requires good memory and knowledge of location (Fig. 1). Secondly, the collection of dispersed food items requires the necessary locomotor skills, important in the case of hominins as they converted from 4-legged walking to two legs. Thirdly, hands are used in the preparation of food in hominins, as in most primates, and the human hand changed little from the morphology present in many fossil apes. Fourthly, mastication of food is related to morphologies of the teeth and jaws, and the enlarged teeth with thick enamel in later Miocene fossil apes and Pliocene and early Pleistocene hominins is a function of their coarse or hard-object diets. Finally, digestion of food and storage of energy is based on the concurrence of genetic and metabolic factors.

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Figure 1
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Five stages in feeding process in human evolutionary history 4.
Fossil apes were frugivorous and both arboreal and terrestrial
The earliest fossil apes emerged in Africa during the early Miocene, approximately 25–18 Ma. These apes represented a marked advance over prior primates and were larger (three to four feet long and weighing 10–60 kg) and with a bigger cranial capacity. These early fossil apes had a gracile skull, low alveolar prognathism, and relatively small teeth. They were pronograde tree-climbers. They have been found associated with both tropical rain forest and tropical woodland environments 1-5 and appear to have been mainly fruit eaters 4 and arboreal within these habitats 5.

Evidence for later fossil apes, 16–8 Ma, is that most known species were associated with deciduous woodlands, both tropical and subtropical, and no evidence of rain forest associations has yet been found. Woodlands differ from tropical forest in that they have single tree canopies, making it difficult if not impossible for animals bigger than squirrels to move from tree to tree without coming to the ground 6. Fossil apes from this period have both arboreal and terrestrial adaptations 7, 8. The woodlands were seasonal, losing their leaves in the off-season, either cold or dry, with most plant species fruiting only once a year 9.

At the beginning of the Middle Miocene, at about 16–15 Ma, there was an increase in global temperature, and at this time, the earliest migration of fossil apes out of Africa reached Turkey and Western Europe. They are associated with subtropical, summer rainfall woodlands, for example at Pašalar, Turkey 10. Later species, probably from a separate migration (see below), are associated with subtropical deciduous woodlands in Spain and Hungary 11, and later still with mixtures of deciduous coniferous woodlands and sclerophyllous evergreen woodlands 12-15. The earliest known hominins at 5-4Ma also lived in tropical deciduous woodland 16-18, and the evidence suggests that this habitat did not differ to any significant degree from that of later Miocene apes.

Shortly after the arrival of apes in Europe, global temperatures dropped sharply, marking a period of aridification and falling temperatures. In Africa, the cooler and more seasonal climate would have had the effect of contraction of equatorial forest and increasing seasonality in woodland habitats, and fossil apes are found not in forest but in seasonal woodland habitats. In Eurasia, the cooling resulted in an increasingly seasonal world in which dry/cold seasons were more extreme and longer 19. As a consequence, fruits that had been the primary food for apes, became hard to find during the cooler months. Evidence for intermittent (likely seasonal) starvation has been found at Pašalar in Turkey 20, and all ape colonies receded to small regions (refugia) until complete extinction occurred in Europe and Asia, approximately 8 Ma. Nevertheless, there is some evidence, based on the fossil record, that some of the European apes may have migrated back to Africa during this time 20-25.

Uricase mutation and its potential impact on human nutrition
The changing climate placed stress on the fossil apes, and rapid changes in genome occurred during this period 26, and there was a complete silencing of the uricase gene in the great ape and human clade 27, 28. The observation that a parallel mutation in uricase occurred somewhat later in Lesser Apes (Hylobatidae) during the late Miocene suggests the mutation provided selection (survival) advantage. The effects of the mutation were to shut down the gene and stop the production of the enzyme uricase 19, 27, the function of which is to break down uric acid.

Uric acid is a metabolic product of purine metabolism, and in most mammalian species, it is metabolized by the enzyme uricase (urate oxidase) to generate allantoin. However, in the great ape and human lineage (Hominidae), a progressive reduction in uricase activity occurred due to mutations in the promoter region followed by complete silencing of the gene from mutations in the coding region of codon 33 of exon 2 28. The genetic shutdown must have preceded the divergence of the orang utan, for the same mutation is present in this Asian great ape as well as the African apes and humans (Fig. 2). The consequence was a rise in serum urate, likely from levels of 1–2 mg dL−1 (based on measurement of uric acid in primates that still carry uricase) to levels of 3–4 mg dL−1 (based on studies of great apes and humans living on native (nonwestern) diets 29.

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Figure 2
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Phylogeny of apes and humans, showing the location of uricase mutation in the common ancestor of the great ape and human lineage and the independent mutation in the gibbon lineage later in time 38.
While several potential hypotheses have been forwarded for why an increase in serum urate may have been beneficial 30, 31, one of the stronger hypotheses is that it may have amplified the ability to store fat and glycogen from fruit sugar (fructose) 19. Recently, it has been shown that where fructose is the nutrient of choice, animals are able to increase their fat stores to protect them from periods where food is not available, such as during hibernation, long-distance migration or nesting 32. Fructose metabolism, unlike other nutrients, lowers energy levels in the cell, triggering adenine nucleotide degradation and uric acid formation that stimulate fat accumulation and insulin resistance 33, 34. The uricase mutation results in more uric acid formation in response to fructose, and this translates into higher blood pressure, a greater increase in liver fat and an increase in gluconeogenesis 28, 35, 36. The ability of the mutation to enhance the ability of fructose to generate fat creates a survival advantage that would be greater in temperate habitats in Eurasia, where dry/cold seasons would have been greater and longer. Thus, the uricase mutation, by amplifying the effects of fructose to increase fat stores, blood pressure and insulin resistance may have acted as a ‘thrifty gene’, providing survival advantage to fossil apes in seasonal habitats during times of food shortage 37.

However, in present human populations, the intake of fructose has increased markedly due to the introduction of refined sugar (sucrose) and the sweetener, high fructose corn syrup. As a consequence of increased sugar (fructose) intake as well as purine-rich foods, such as meat, serum urate is now between 3 and 12 mg dL−1, and those with the higher levels are at increased risk for developing type 2 diabetes, obesity, fatty liver and hypertension 38. Consistent with these findings, pilot clinical studies suggest reduction in fructose intake 39-41, or a lowering of serum uric acid, may improve features of metabolic syndrome, including blood pressure, insulin resistance, fatty liver and weight 42-44.

Evolutionary adaptations to famine are likely to affect nutrition and metabolic outcomes 29. On the other hand, the ‘weather hypothesis’ proposes that animals evolved to withstand periods of starvation by changing life history strategies to undergo regular periods of calorie restriction 45. By this means, lifespan could be maintained or even increased 46-48. For example, data on time spent hibernating in Turkish hamsters suggest that hibernation in small mammals retards biological ageing in proportion to the amount of time spent in the hibernating state 49. For animals that do not hibernate, periods of calorie restriction would be a regular feature in seasonal habitats, with animals losing more than half their body weight in winters, and the ‘weather hypothesis’ proposes that this is a biological or evolutionary strategy rather than necessity imposed by occupation of strongly seasonal habitats. As prolonged periods of fasting activate Nrf2 in animals 50 and man 51, it can be hypothesized that up-regulation of this anti-inflammatory cytoprotective transcription factor may contribute to the survival advantage in species that undergo fasting.

Early hominins: adaptations for bipedalism
The evolution of bipedalism has often been assumed to be due to leaving the shelter of forest and woodland and coming down to the ground, and it has been further assumed that upright posture was both a necessary pre-adaptation for bipedalism and itself an indication of its presence. The former may be true, but the latter is clearly not, for upright posture is present in many fossil apes that manifestly were not bipedal. Upright posture is seen in adaptations of the axial skeleton, such as reduction in lumbar vertebrae, broadening of the chest and long clavicle, and these are character states present in some later Miocene apes and all hominids, that is the great apes and humans. The earliest adaptations for bipedalism in human ancestry took place in deciduous woodlands, similar to those occupied by fossil apes for the 5 to 9 million years previous to the appearance of hominins 16, 17, 52, 53. Seasonal climates and diets composed largely of fruit were retained in the earliest hominins 18.

The present evidence suggests that adaptations of the hip and feet were amongst the earliest to change at 4-3Ma 54-57. Even after broadening of the ilium in Ardipithecus ramidus 58, the foot from the same individual 59 still retained a divergent and grasping big toe. Similarly, lengthening of the legs had not taken place in early hominins and the earliest evidence is on the australopithecine called ‘little foot’ at 3.6 Ma in South Africa 55, 56, where leg length exceeded arm length (Fig. 3). Human striding ability was not fully established until 1.8–2.0 Ma with the appearance of Homo erectus.

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Figure 3
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The skeleton of STW573 from Sterkfontein 56. Copyright paul john myburgh (with permission).
Bipedalism may have provided some evolutionary benefits other than as a form of locomotion, such as the fact that an upright posture may have been improved heat control by reducing exposure to sun and enabled long-distance running 60-63. On the other hand, if bipedalism evolved in woodlands, not savannah, heat stress would not have been significant. Four-footed canid species are able to run down their prey over long distances, and so that these features of bipedalism would seem to be side effects rather than a major contributing factor in the evolution of bipedalism. Its major evolutionary advantage is that the forearms are released from their locomotor function and hands become free for other uses.

Many animals use their ‘hands’ for feeding, for example most rodents, many carnivores and all primates, but use is restricted because nearly all of them use all four legs for locomotion. Freed from locomotor function, mobile arms and prehensile hands (long thumbs and short fingers) are essential feeding tools for fossil apes and hominins at all stages of evolution. All fossil apes as known at present had long thumbs and had a form of precision grip analogous with that of hominins, such as Ardipithecus ramidus. However, known fossil apes had nonrotatory joints of the thumb 64, but the human thumb rotates at its joint to form the uniquely human precision grip between thumb and fingers 65, 66. The human precision grip is unique to humans, and its function is dependent on freeing of the hands from locomotor function.

Bipedalism and dietary change
Most of the evolutionary developments of bipedalism and freeing of the hands are interlinked, and all are linked with the environment and diet. They did not, however, all occur at once. The earliest hominins lived in similar environments and had similar diets to those of fossil apes 67, 68, in both cases with low quantities of animal products being eaten, as in living chimpanzee populations 69-71: chimpanzees hunt and eat smaller animals, providing survival value during dry seasons when fruit is scarce 69-73. However, the quantity of animal products in chimpanzee diet is below 10% and, thus, below the threshold of omnivory. It is likely that the last common ancestor of chimpanzees and humans also ate some animal products, and since early hominins remained in the same woodland environment as fossil apes and still remained dependent on trees for food and shelter, it is likely that this diet remained with little change for the first few million years of human evolution (5–3 Ma) 53.

At 3 to 2 Ma, major evolutionary changes occurred in hominin diets. During this time, there was another period of global cooling 74, 75 and the formation of the rift valleys 76, which brought about changes in wind and water flow across the continent 1 and increasing climatic seasonality. This had a major impact on animals depending on fruit for the main part of their diet, resulting in reduced availability of fruit during the drier or cooler months, and even fall-back foods, such as leaves and bark becoming scarce. Figs would have partly mitigated the seasonal shortages 77 and no doubt scattered fig trees would have been highly prized 53. Evidence of dietary stress is seen in the teeth of fossil apes living 15 Ma in Turkey, some of which have prominent hypoplastic lines (Fig. 4), formed during periods of disease or starvation, and patterns of cyclical growth/stasis have also been found in South African australopithecines, also attributed to seasonal changes in food availability 78.