Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology
ReviewBrain-specific lipids from marine, lacustrine, or terrestrial food resources: potential impact on early African Homo sapiens☆
Introduction
Many previous authors have considered human evolution from an ecological view point (Martin, 1983, Harvey and Clutton-Brock, 1985, Shipman and Walker, 1989, Blumenschine, 1991, Foley and Lee, 1991, McHenry, 1994, Aiello and Wheeler, 1995, Leonard and Robertson, 1997, Ambrose, 1998, Broadhurst et al., 1998). They have argued that the relatively large metabolic energy requirements of the Homo (mainly H. sapiens) brain require consistent access to higher quality food resources, both now and in the past. Regardless of the various selective pressures driving brain evolution of H. sapiens, sufficient dietary energy, protein, vitamins, and trace elements are strictly required. Particularly in tropical and sub-tropical climates, these nutrients can be obtained from many food resources that hominids could have accessed (Harris and Ross, 1987, O'Dea, 1991, Eaton et al., 1996, Eaton et al., 1997). All land based mammals had access to this range of nutrients as is testified by the large body masses and fast growth rates they attained. The problem with this approach, is that despite achieving velocities of body growth approaching a ton in four years, the rule was a logarithmic decline in brain to body weight ratio with increase in body size.
Whilst proteins are important to body growth, 60% of the brain structural material (dry weight) is lipid. Different principles are required for body growth as opposed to brain growth. Dietary essential long-chain polyunsaturated fatty acids (LC-PUFA) are considered to be the most limiting nutrients for brain lipids and neural growth (Crawford and Sinclair, 1972, Hornstra et al., 1995, Crawford et al., 1993, Crawford et al., 1997, Broadhurst et al., 1998, Clandinin, 1999, Horrobin, 1999), and are not widely available in foods. Sustaining the comparatively large size, and the apparent unique complexity and high level of interconnectivity in the modern human brain require LC-PUFA (Mesulam, 1990, Fernstrom, 1999, Horrobin, 1999).
Very rapid brain growth characterizes the modern human fetus and neonate, who devote approximately 70% of their metabolic energy to fuel central nervous system (CNS) growth and development (Holliday, 1971, Cunnane et al., 2000). In the fetus and neonate both the quality and quantity of nutrients—especially LC-PUFA, iodine and other trace elements, are critically important. Normal intellectual growth cannot be accomplished if any of these are lacking. Adult human brains require approximately 20% of metabolic energy, a large figure compared to other mammals of the same size (Leonard and Robertson, 1997, Crawford et al., 1993, Broadhurst et al., 1998, Dutta-Roy, 1997, Clandinin, 1999).
Due to these strict energetic constraints on H. sapiens, evolutionary models should consider quantitatively the sources of LC-PUFA in representative marine, lacustrine, riverine and terrestrial animal foods that may have been procured by hominids and delivered LC-PUFA. The archaeological evidence for the utilization of littoral resources by Homo during the period 20–200 kya is of increasing interest and significance.
Section snippets
Brain-specific nutrition must provide balanced dietary LC-PUFA
The lipid of the mammalian brain has a unique profile of LC-PUFA (Crawford and Sinclair, 1972, Crawford et al., 1976a). The highly unsaturated LC-PUFA is found in neuronal and retinal membranes at sites of high signal transfer activity. Membranes with higher amount of saturated fatty acids are found in more rigid structures such as those of the insulating myelin sheaths around nerves.
PUFA are ‘essential’, which means that they cannot be synthesized and must come from the diet. There are two
Maternal investment and fetal and neonatal growth determine intellectual capacity
Apart from the need for DHA, there is also a need for AA in the brain, placenta, internal organs, and blood vessels. AA is a major structural component of the endothelial cells that line blood vessels. The placenta is basically a very rapidly growing blood vessel matrix that processes great and increasing volumes of blood during pregnancy. High levels of AA are necessary to construct this blood vessel matrix. AA is also the substrate for the eicosanoid hormones that are involved in the blood
Marine and lacustrine sources of LC-PUFA
The evolution of the visual and nervous system occurred in the early proto-ocean environment some 600 million years ago. The first visual systems used what is now called vitamin A as the photon sensitive molecule with docosahexaenoic acid (DHA) as the main constituent of the lipid support for the protein and photo-transduction system. These molecules would have been present in abundance, having been produced by the algae which had dominated the proto-oceans for some 2.5 billion years
Brain specific nutrient cluster includes iodine, vitamin A and anti-oxidants argues against an inland evolution of H. sapiens
It is evident that other nutrients occurred in the food chain quite specifically with DHA. These nutrients form a cluster which are at their richest in the marine food chain. They are vitamin A and trace elements. For example, iodine deficiency disease and mental retardation is found in high prevalence amongst inland cultures. Dobson (1988) has discussed a plausible role for iodine in cerebral evolution and the separation of Cro-Magnon from the Neandertals. Dobson presents the case that the
The wealth and ease of harvesting of the littoral food chain
The marine food chain consistently provided the DHA necessary for the origin and evolution of simple and then the advanced neural and visual systems. Fish and shellfish lipids from lower latitudes and/or fresh water are excellent sources brain-specific nutrition, since they provide a rich, balanced source of DHA. They also provide AA necessary for vascular development, which is essential for the provision of the disproportionately high energy requirement needed by the brain (Table 1, and
Terrestrial sources of brain-specific nutrition
Brain-specific nutrition would have required a balanced source of both DHA and AA to provide the greatest advantage for cerebral expansion. Whilst the littoral food chain would have offered this advantage, the muscle meat and organs of large savannah herbivores would not (Crawford et al., 1976a, Crawford et al., 1976b). Small mammals are able to accumulate DHA consistent with their high brain to body weight ratios (which can be greater than the 2% of H. sapiens (Table 3). Thus, a small
Early modern humans in South Africa
The fossil and mitochondrial DNA evidence thus far supports an African origin for modern humans (Nitecki and Nitecki, 1994, Stringer and McKee, 1997). Lakeshore sites in the Rift Valley have yielded fairly sophisticated stone tools as old as 260 kyr associated with H. sapiens remains with varying mixes of archaic and modern traits (Clark, 1992). The Singa hominid (Sudan), considered to be postcranially robust but otherwise anatomically modern H. sapiens dates to circa 190 kyr (McDermott et al.,
Shell middens in the Cape MSA
Along the Cape West and South coasts there are many MSA sites with abundant shellfish and other marine food remains; the total number of sites may be in the hundreds (Fig. 2). The best known of these coastal sites is at Klasies River Mouth, where over 20 m depth of shell midden has accumulated, much of it dating to oxygen isotope stage 5 (Grun et al., 1990b, Deacon, 1992). Recently the shell middens in a small cave at Blombos have been dated to 80–100 kyr (Henshilwood and Sealy, 1998). Some
The Middle East
Shell and fish bone middens of phenonmenal scale dating to 40 kyr are found at over 40 sites along the Nile River Valley leading out of Africa into the Middle East (Stewart, 1989, Stewart, 1994). The remains provide evidence for seasonal fishing camps that were frequented year after year. These archaeological data are have been used to define modern human behavior at a site, but this corridor was in use long before 40 kya (Van Peer, 1998), and perhaps the fishing sites were, too. Walter et al.
Overview
All land based mammals, without exception, lost relative brain capacity logarithmically as they evolved larger bodies. The fast growth rate in these species outstrips their capacity to synthesise the LC-PUFA required for the brain and there is no significant source of these essential nutrients in the savannah food chain. There is no science-based evidence which would explain H. sapiens being an exception to this rule of brain capacity loss with increase in body size. The outstanding feature of
Conclusion
In this paper we have attempted to discuss nutritional resources that could have contributed to an increase in intellectual capacity and creativity without relying on pre-exisiting modern behavior. Future excavations and resource modelling would benefit from quantitative treatment of the sources of brain-specific nutrition that hominids may have accessed. However, an evidence-based approach is essential. There is now robust evidence on the absolute requirements of brain growth for the omega
References (157)
- et al.
Non-methylene interrupted fatty acids in lipids of shallow water marine invertebrates: a comparison of two molluscs (Littorina littorea and Lunatia triseriata) with the sand shrimp (Crangon septemspinosus)
Comp. Biochem. Physiol.
(1973) - et al.
Total lipids and nutritionally important fatty acid products of some Nova Scotia fish and shellfish products
Can. J. Food Sci. Technol.
(1988) Late Pliestocene bottlenecks, volcanic winter, and differentiation of modern humans
J. Hum. Evol.
(1998)Nutritional and hormonal factors influencing desaturation of essential fatty acids
Prog. Lipid Res.
(1981)- et al.
Hunting and scavenging by Plio-Pleistocene hominids: nutritional constraints, archeological patterns, and behavioral implications
J. Archeol. Sci.
(1993) - et al.
Plant–animal subsistence ratios and macronutrient energy estimations in worldwide hunter-gatherer diets
Am. J. Clin. Nutr.
(2000) The placental delivery of arachidonic and docosahexaenoic acids: implications for the lipid nutrition of the preterm infant
Am J Clin Nutr.
(2000)- et al.
Comparative studies on fatty acid composition of wild and domestic meats
Int. J. Biochem.
(1970) - et al.
Muscle and adipose tissue lipids of the warthog, Phacochoerus Aethiopicus
Int. J. Biochem.
(1970) - et al.
The long chain metabolites of linoleic and linolenic acids in liver and brains of herbivores and carnivores
Comp. Biochem. Physiol.
(1976)
Essential fatty acids and fetal brain growth
Lancet
Are deficits of arachidonic and docosahexaenoic acids responsible for the neural and vascular complications of preterm babies?
Am. J. Clin. Nutr.
The majority of dietary linoleate in growing rats is α-oxidized or stored in visceral fat
J. Nutr.
Substantial carbon recycling from linoleate into products of de novo lipogenesis occurs in rat liver even under conditions of extreme dietary linoleate deficiency
J. Lipid Res.
Long-chain polyunsaturated fatty acids in children with severe protein-energy malnutrition with and without human immunodeficiency virus-1 infection
Am. J. Clin. Nutr.
Fatty acid transport and metabolism in the feto-placental unit and the role of fatty acid binding proteins
Nutr. Biochem.
An evolutionary perspective enhances understanding of human nutritional requirements
J. Nutr.
Use and storage of carbohydrate and fat
Am. J. Clin. Nutr.
Additional human fossils from Klasies River Mouth, South Africa
J. Hum. Evol.
Human remains from Blombos Cave, South Africa: 1997–1998 excavations
J. Hum. Evol.
A replication study of violent and nonviolent subjects: cerebrospinal fluid metabolites of serotonin and dopamine are predicted by plasma essential fatty acids
Biol. Psychiatry
Dietary polyunsaturated fatty acids and depression: when cholesterol does not satisfy
Am. J. Clin. Nutr.
Essential fatty acid status in pregnancy and early human development
Eur. J. Obs. Gyn. Rep. Biol.
The membrane phospholipid hypothesis as a biochemical basis for the neurodevelopmental concept of schizophrenia
Schizophr. Res.
Correlation between level of (n−3) polyunsaturated fatty acids in brain phospholipids and learning ability in rats. A multiple generation study
Biochim. Biophys. Acta
Paleoenvironmental and human behavioral implications of the Boegoeberg 1 Late Pleistocene hyena den, Northern Cape Province, South Africa
Quat. Res.
Placental essential fatty acid transport and prostaglandin synthesis
Prog. Lipid Res.
Long chain polyunsaturated fatty acids in fetal growth
Early Hum. Dev.
Dietary protein requirements in athletes
J. Nutr. Biochem.
Fatty acid composition of brain, retina, and eryythrocytes in breast- and formula-fed infants
Am J. Clin. Nutr.
The arachidonic acid content of the Australian diet is lower than previously estimated
J. Nutr.
A critique of the evidence for scavenging by Neandertals and early modern humans: new data from Kobeh Cave (Zagros Mountains, Iran) and Die Kelders Cave 1 Layer 10 (South Africa)
J. Hum. Evol.
New Late Pleistocene uranium–thorium and ESR dates for the Singa hominid (Sudan)
J. Hum. Evol.
Marine Biogenic Lipids
Lowering of eicosanoid formation, amelioration of clinical symptoms and laboratory findings in patients with rheumatoid arthritis on a vegetarian diet
Arachidonic acid to eicosapentanoic acid ratio in blood correlates positively with clinical symptoms of depression
Lipids
The expensive tissue hypothesis. The brain and digestive system in human and primate evolution
Curr. Anth.
Maternal essential fatty acid patterns during normal pregnancy and relationship to neonatal essential fatty acid status
Br. J. Nutr.
Visual acuity, erythrocyte fatty acid composition, and growth in term infants fed formulas with long chain polyunsaturated fatty acids for one year. Ross Paediatric Lipid Study
Pediatr. Res.
The 1992–1993 excavations at the Die Kelders Middle Stone Age site, South Africa
J. Field Archaeol.
A randomized controlled trial of early dietary supply of long-chain polyunsaturated fatty acids and mental development in term infants
Dev. Med. Child. Neurol.
Visual acuity and the essentiality of docosahexaenoic and arachidonic acid in the diet of term infants
Pediatr. Res.
Hominid carnivory and foraging strategies, and the socio-economic function of early archaeological sites
Philos. Trans. R. Soc., Lond. B
Scavenging and human evolution
Sci. Am.
Balanced intakes of natural triglycerides for optimum nutrition: an evolutionary and phytochemical perspective
Med. Hypotheses
Rift Valley lake fish and shellfish provided brain specific nutrition for early Homo
Br. J. Nutr.
Dating and context of three Middle Stone Age sites with bone points in the Upper Semliki Valley, Zaire
Science
Utilization of lipids during exercise in human subjects: metabolic and dietary constraints
Br. J. Nutr.
Health survey of the El Molo
E. Afr. Med. J.
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This paper was presented by MAC at the Year 2000 Great Unknowns Symposium, Cambridge, UK.