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Brain-specific lipids from marine, lacustrine, or terrestrial food resources: potential impact on early African Homo sapiens

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Abstract

The polyunsaturated fatty acid (PUFA) composition of the mammalian central nervous system is almost wholly composed of two long-chain polyunsaturated fatty acids (LC-PUFA), docosahexaenoic acid (DHA) and arachidonic acid (AA). PUFA are dietarily essential, thus normal infant/neonatal brain, intellectual growth and development cannot be accomplished if they are deficient during pregnancy and lactation. Uniquely in the human species, the fetal brain consumes 70% of the energy delivered to it by mother. DHA and AA are needed to construct placental and fetal tissues for cell membrane growth, structure and function. Contemporary evidence shows that the maternal circulation is depleted of AA and DHA during fetal growth. Sustaining normal adult human brain function also requires LC-PUFA.

Homo sapiens is unlikely to have evolved a large, complex, metabolically expensive brain in an environment which did not provide abundant dietary LC-PUFA. Conversion of 18-carbon PUFA from vegetation to AA and DHA is considered quantitatively insufficient due to a combination of high rates of PUFA oxidation for energy, inefficient and rate limited enzymatic conversion and substrate recycling. The littoral marine and lacustrine food chains provide consistently greater amounts of pre-formed LC-PUFA than the terrestrial food chain. Dietary levels of DHA are 2.5–100 fold higher for equivalent weights of marine fish or shellfish vs. lean or fat terrestrial meats. Mammalian brain tissue and bird egg yolks, especially from marine birds, are the richest terrestrial sources of LC-PUFA. However, land animal adipose fats have been linked to vascular disease and mental ill-health, whereas marine lipids have been demonstrated to be protective. At South African Capesites, large shell middens and fish remains are associated with evidence for some of the earliest modern humans. Cape sites dating from 100 to 18 kya cluster within 200 km of the present coast. Evidence of early H. sapiens is also found around the Rift Valley lakes and up the Nile Corridor into the Middle East; in some cases there is an association with the use of littoral resources. Exploitation of river, estuarine, stranded and spawning fish, shellfish and sea bird nestlings and eggs by Homo could have provided essential dietary LC-PUFA for men, women, and children without requiring organized hunting/fishing, or sophisticated social behavior. It is however, predictable from the present evidence that exploitation of this food resource would have provided the advantage in multi-generational brain development which would have made possible the advent of H. sapiens. Restriction to land based foods as postulated by the savannah and other hypotheses would have led to degeneration of the brain and vascular system as happened without exception in all other land based apes and mammals as they evolved larger bodies.

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

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    This paper was presented by MAC at the Year 2000 Great Unknowns Symposium, Cambridge, UK.

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