A SHORE-BASED DIET RICH IN ENERGY AND ‘BRAIN-SPECIFIC’ NUTRIENTS MADE HUMAN BRAIN EVOLUTION POSSIBLE:
Proceedings of the Ghent Conference on Water and Human Evolution
Stephen C. Cunnane
Department of Nutritional Sciences, University of Toronto
The Modern Human Brain
The modern adult human brain has a volume of about 1300-1400 cm3. This is 3-5 fold larger than that of extant primates, 2-3 fold larger than that of Australopithicines and early Homo and as much as ten fold larger than in non-primate animals of similar size to adult humans. Brain expansion began gradually but accelerated significantly in the last 500,000 years. The origin of this key feature of modern humans has not been satisfactorily explained. It has been recognized elsewhere that the brain of all animals has a disproportionately high metabolic rate relative to other organs. Other factors being equal, a large-brained human requires a diet with higher energy density than an animal of similar size but with a smaller brain.
Generally, evolutionists attempt to explain hominid brain expansion by invoking ‘need’ or ‘advantage’; the larger brain would need more energy so a better quality diet would be sought out resulting in more fat and meat consumption, or the larger brain was advantageous for tool-making, language, or socialization. If brain expansion were simply a matter of diet selection or intellectual advantage, why did a similar degree of brain expansion relative to body weight not occur in other primates or in other mammals?
It is impressive enough that adult human brains occupy about 2% of body weight and are 3-5 fold larger than those of adult primates. However, proportionately, the human brain is much larger at birth (12-14% of body weight) and consumes upwards of 70% of the body’s energy intake. Furthermore, the frequent comparison to body weight is between a species that is relatively fat (humans) and other terrestrial mammals which are virtually all lean. Hence, on a lean body basis, the modern human brain/body weight ratio is comparatively even larger.
Interestingly, the brain/body weight ratio in the modern human infant at birth is not very different from that of other primates such as gibbons, suggesting that, as fetuses, all primates have the potential to achieve the brain development of humans. Human learning is a remarkable but slow process representing considerable evolutionary and metabolic investment in an organ that contributes little to its owner’s survival for several years. These are some of the remarkable features of the modern human brain that bear explanation.
Nutrition and Brain Function
Undernutrition adversely affects brain function in developing mammals from laboratory rodents to humans. Undernutrition has two main components – insufficient energy intake and insufficient intake of essential nutrients, i.e. nutrients that the body cannot make at all or cannot synthesize in sufficient quantities to meet its needs. When present during the ‘critical phase’ of brain development (first five years in humans), either of these components of undernutrition alone can permanently impair brain function in all mammals including humans. Undernutrition contributes significantly to the increased incidence of neurodevelopmental problems experienced by low birth weight infants and those born prematurely.
In laboratory settings it is possible to distinguish between the impact of energy deficit per se and the deficit of specific nutrients whereas in the ‘field’ this distinction rarely operates. However, the key benefit of studying specific nutrient deficiencies is that one can determine those that are more limiting for brain development from those that are less limiting. This gave rise to the concept of ‘brain-specific’ nutrients, coined by Cunnane et al (1993). While no nutrients are required specifically by the brain, the deficiencies of some nutrients affect the brain more than other organs, especially during early development. The list includes n-3 polyunsaturated fatty acids, iodine, copper and iron; deficiency of any one of these nutrients alone causes reproducible and often permanent impairment in neurodevelopment that can be prevented by inclusion in the diet of sufficient amounts of that nutrient. The point is that an energy-rich diet was necessary but, alone, was insufficient to promote hominid brain expansion. In addition to abundant dietary energy supply, an abundant supply of ‘brain-specific’ nutrients was an absolute requirement as demonstrated by the ongoing vulnerability of the modern human brain to their deficiency in the diet (see later).
Nutrients, especially essential minerals such as iodine, copper and iron, are not distributed evenly in the earth or between land and water. Hence, the quality of the local food supply can be a major determinant of health and it is not unusual for plants and animals to encounter soil or nutritional deficiencies that prevent normal reproduction or development. In relation to human brain function, perhaps the best example is iodine deficiency.
Iodine deficiency is now well known in Western societies and is preventable by supplementation via iodized table salt. This was not always the case and is still not the case in many areas of the world. As a result, over 1.5 billion people worldwide have iodine deficiency, one of the symptoms of which is mental retardation. The role of iodine in energy metabolism and the reason mental retardation occurs in iodine deficiency are not understood. However, without iodized salt, the majority of Western society would still be plagued by iodine deficiency. In fact, concern is re-emerging in Britain that sub-clinical iodine deficiency may be present especially in vegetarians and those on reduced salt intake for hypertension. However, those that consume seafood do not face this problem because iodine is more plentiful in shore-based foods, especially shellfish and fish, than in the inland terrestrial food supply.
The role of iodine in brain function is especially relevant to human brain evolution because the savannah or woodland environment usually purported to be the niche for emergence of humans provides a diet low in iodine. This predominantly vegetarian diet is not exceedingly iodine deficient, but, as we have proposed before (Cunnane et al 1993), it is low enough to potentially limit brain expansion and it is low enough to give renewed concern about iodine deficiency in modern societies.
Normal development of the mammalian brain and eye depends on adequate accumulation a long chain n-3 polyunsaturated fatty acid with six methylene-interrupted double bonds – docosahexaenoate (DHA) - in the membranes of those organs. Exactly what DHA does is not fully understood but it cannot be replaced by any other molecule, even very similar fatty acids with five double bonds (Crawford et al,1999). DHA has traditionally been viewed as not technically being ‘essential’ in the diet because it can be synthesized endogenously; the pathway exists in all mammals studied to date. The critical point is that the capacity to synthesize DHA in human infants appears from recent studies to be insufficient to provide the amounts of DHA needed for normal brain accumulation of DHA or for normal brain and visual development. Hence, DHA is becoming accepted as conditionally essential, at least for neonates, a concept already well established in nutrition.
DHA is not present in terrestrial plants. It is virtually absent from animal fat and it is only present in low amounts in meat. It is present in plentiful amounts in shellfish and fish. Hence, like iodine, DHA is a ‘brain-specific’ nutrient that is limiting for optimal brain development and is in very short supply from the inland terrestrial food chain but is readily obtained from shore-based foods or fish. DHA is present in human breast milk but this source is strictly dependent on maternal DHA intake although low levels are present even in milk of vegetarians. Nevertheless, the uniquely human experiment of feeding infants artificial milk formulas has demonstrated that infants not receiving dietary DHA have about 50% less brain DHA than those that are breast fed; this deficit occurs despite the presence of DHA in infant fat stores at birth.
Neonatal Fat Stores
Amongst terrestrial mammals, most healthy humans have a significant layer of subcutaneous fat usually accounting for 20-30% of body weight. The degree of adiposity varies greatly in adults, largely according to lifestyle, but is a much more consistent feature of healthy term infants. Human infants appear to be unique among terrestrial mammals in being born with about 500-600 g of body fat (about 15% of body weight). After birth, this fat store continues to increase to about 2000 g at about six months of age. However, its fatty acid profile markedly changes from birth when the long chain polyunsaturates are at the highest point (about 1% of all fatty acids), to adulthood, when the long chain polyunsaturates are low to nonexistent. Before birth, fat accumulation occurs primarily during the third trimester. Hence, infants born ten weeks prematurely have about 10% of the fat stores of term infants. Low birth weight infants typically undergo intrauterine growth retardation and are also born with low fat stores.
Body fat is an energy store . Between meals, free fatty acids are liberated from fat and b-oxidized for energy. They are also converted to ketones, which are produced when the capacity to b-oxidize fats exceeds the capacity to utilize the resulting acetyl CoA. Like glucose or free fatty acids, ketones can also be converted to acetyl CoA. In adult humans, this usually occurs when glucose supplies are depleted and is essential as an alternate fuel for the brain during fasting or starvation.
Body fat is not simply ‘acquired’; metabolically, its costs a lot to produce and is not sustained without at least a balance between energy intake and expenditure. Few, if any, morphological features of humans are as dependent on diet as adiposity, especially at birth. Attempting to explain its potential advantages in modern humans (buoyancy, insulation, protection against starvation) does not explain its origin which requires high energy density in the diet and/or sustained inactivity. Deposition of body fat does not necessarily require consumption of large amounts of fat; low fat diets rich in rapidly absorbed carbohydrates markedly increase fat synthesis in humans. Activity levels also affect fatness, independent of the energy density of the diet.
Ketones and Brain Lipid Synthesis
Infants typically have higher blood ketones than adults. In studies with animals, ketones appear to be more readily taken up and utilized by the infant than adult brain. In addition to being an alternate fuel, ketones are also a primary source of carbon for brain lipid synthesis; in fact, in humans and rats, they appear to be more important than glucose in this role. Lipids constitute about 50% of the dry weight of the brain and cholesterol represents about half that total. Cholesterol and all fatty acids except the long chain polyunsaturates in the brain have got to be synthesized in situ; these lipids are not imported from the circulation. Details of this process and its implications have been published elsewhere (Cunnane et al, 1999). Hence, a reliable source of carbon for this very active stage of brain lipid synthesis is crucial. If glucose were the predominant fuel for the brain, it would make sense for the predominant substrate for lipid synthesis to be something different, like ketones, especially in a large-brained species. It would make even more sense if there were a substantial supply of ketone substrate in the form of body fat.
The link between infant fat stores, ketones, lipid synthesis and human brain evolution is that something had to provide a reliable and very long term supply of the additional dietary energy for fat deposition on the third trimester human fetus during pregnancy. This fat store at birth would be added to during postnatal development so that brain energy and lipid requirements could be expanded. Other primates do not have this fat depostion during fetal and neonatal development and I argue that this is a critical limitation on postnatal brain development and evolution. Advantages of buoyancy and possibly insulation are secondary and, regardless of them or the ‘requirements’ of the expanding hominid brain, dietary supply of energy is the central issue. What diet could have reliably provided this abundance, indeed excess, of energy for over 500,000 years of human evolution, thereby ensuring significant fat deposition in utero?
This brain metabolism/evolution scenario requires a diet that is abundant in energy and contains ‘brain-specific’ nutrients. What are the options? Woodland habitats provide an abundance of fruits and vegetables. Some of these, especially ripe nuts, are rich in energy but virtually all other plants are extremely low in fat. None of them have DHA and iodine is relatively low. The high fiber content generally limits availability of all the essential minerals. Woodlands also have many types of animals and birds; some of the animals are potential prey and some are predators. Survival and competition would become key issues. Fat deposition would remain at a premium especially if foraging and hunting were necessary. Savannahs offer no nutritional advantages over woodlands; if anything, diversity in the edible plant food supply is more limited on the savannah and the energy-rich foods like nuts would be almost non-existent. In my view, ‘survival’ and brain human expansion were incompatible; brain expansion had to be accomplished under long term conditions of food abundance and the absence of any serious survival challenges.
The habitat proposed that would have permitted hominid brain expansion is the shorelines of major lakes, estuaries and the sea in temperate and equatorial zones (Cunnane et al 1993, Crawford & Marsh 1995, Broadhurst et al 1998). Prior to the destructive exploitation of modern times, such shorelines had an almost limitless abundance of shellfish. Such shorelines with plentiful shellfish skill exist in remote areas including the Queen Charlotte Islands off Canada’s west coast. Seasonally, bird and perhaps reptile eggs would be available. Marsh plants, fruits and vegetables would be abundant. The shellfish and eggs contain the rich energy and nutrient density needed for fat deposition and brain expansion. These foods would require practically no skill to find and no significant preparation to consume. In my view, this lack of urgency was essential to initiate the process of tool development.
As hand-eye coordination improved and more sophisticated thinking emerged, foods more challenging to catch, such as slow moving fish, crustaceans, amphibians, reptiles, and young birds or mammals would all become accessible. As tool making developed, the idea for and ability to set snares, traps and nets would expand both skills and food choices while never becoming essential to provide an adequate food supply. Eventually, bigger game and a wider foraging range would have been manageable while all the time remaining optional. In hominids that ventured over generations into areas where the food and nutrient supply was more limiting, fat deposition would have been at risk and brain expansion would not have continued.
The Rift Valley
The modern day Rift Valley is adjacent to some large lakes that were very much larger when hominid brain expansion was occurring. This sort of location would, in my view, have supported human brain expansion under the necessary conditions described here. Recent fossil finds in South Africa refute the old argument that hominid fossils have not been found in conjunction with fossils of shore-based foods, especially shellfish.
Ongoing Vulnerability – Testing the Hypothesis
The shore-based hypothesis of human brain evolution states that a combination of high dietary energy density and abundant supply of ‘brain-specific’ nutrients made human brain evolution possible. This hypothesis has been tested on many occasions in laboratory animals and in humans; remove energy and ‘brain-specific’ nutrients from the diet and observe the adverse effects within one generation or over several generations. Low birth weight and premature infants have markedly increased risk of neurodevelopmental delay (Crawford & Marsh, 1995). This arises from multiple factors including minimal to non-existent body fat at birth and the difficulty of providing nutrition equivalent to that normally acquired via the placenta while in utero. Even in healthy term infants with appropriate energy intake, lack of pre-formed dietary DHA impairs brain accumulation of DHA, retards neurodevelopment and affects learning in school-aged children (Broadhurst et al 1998, Crawford et al 1999).
Deficient intake of dietary energy and/or ‘brain-specific’ nutrients including n-3 polyunsaturates, iodine, iron, and copper in animal models results in reproducible deficits in neurological and behavioural development, deficits which, in turn, hamper normal mating, reproduction and development in subsequent generations subsisting on the same inadequate diet. These observations clearly demonstrate that human brain maturation pre- and postnatally is still vulnerable to dietary inadequacies which, over generations, would be apparent throughout the affected population.
There are many challenging aspects to explaining human evolution including the origin of anomalous features such as the large brain, diving reflex, bipedalism, relative hairlessness, subcutaneous fat (especially in neonates) and development of speech. The shore-based hypothesis views at least two of these features (neonatal subcutaneous fat, large brain) as being dependent on nutrition. Animals including primates do not develop these features on terrestrial diets but do on shore-based or aquatic diets. A fully aquatic habitat would not be necessary to derive the benefits of the shore-based food supply. However, positioned as it is between the two extremes of fully terrestrial or fully aquatic evolution, a shore-based existence would permit humans to evolve in near constant contact with water or quite remote from it. It would support the development of bipedalism (through enhanced buoyancy, especially in infants) and could plausibly promote hairlessness and development of speech.
The Aquatic Hypothesis has been criticized for superficially attempting to explain too many features of human evolution. The shore-based hypothesis only attempts to explain human brain evolution and, in parallel, neonatal fat stores. In so doing, it accounts for the known and ongoing vulnerability of the human brain and neonatal fat stores to undernutrition. Competing hypotheses need to explicitly address these important physiological and metabolic limitations or explain clearly why they are not relevant; otherwise, they are untenable.
Many discussions with Michael Crawford, Leigh Broadhurst and Tom Brenna have helped formulate this concept over the years. Sir Alistar Hardy and Elaine Morgan provided the forum in which this concept belongs. My own wholly original contribution to this hypothesis of human brain evolution has been the incorporation of the critical role of body fat deposition in neonates and aspects to do with brain lipid synthesis.
Broadhurst, CL, Cunnane, SC & Crawford, MA. 1998. Rift Valley lakefish and shellfish provided brain-specific nutrition for early Homo. British Journal of Nutrition, 79, 3-21.
Cunnane, SC, Harbige, LS & Crawford, MA. 1993. The importance of energy and nutrient supply in human brain evolution. Nutrition and Health, 9, 219-235.
Cunnane, SC, Menard, CR, Likhodii, SS, Brenna, JT & Crawford, MA. 1999. Carbon recycling into de novo lipogenesis is a major pathway in neonatal metabolism of linoleate and a-linolenate. Prostaglandins, Leukotrienes and Essential Fatty Acids, in press.
Crawford, MA, Bloom, M, Broadhurst, CL, Schmidt, WF, Cunnane, SC, Galli, C, Gehbremeskel, K, Linseisen, F, Lloyd-Smith, J. & Parkington, J. 1999. Evidence for the unique function of docosahexaenoic acid during the evolution of the modern hominid brain. Lipids, in press.
Crawford, MA & Marsh D. 1995. Nutrition and Evolution. Keats Publishing, New Canaan, CT.
Additional link: Omega3 depletion and schizophrenia
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