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).
Brain-Specific
Nutrients
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.
n-3
Polyunsaturates
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?
Shore-based
Evolution
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.
Conclusion
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.
Acknowledgements
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.
References
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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