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Bioscience
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Vol. 25, No. 1. pp 1-8
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Human Evolution, Nutritional Ecology and
Prebiotics in Ancient Diet
Jeff D. Leach1, Glenn R Gibson2,
and Jan Van Loo3
1
Paleobiotics Lab, USA,
2The
University of Reading, UK,
3Orafti,
Belgium
Abstract
Modern studies of prebiotic
non digestible carbohydrates continue to expand and demonstrate their
colonic and systemic benefits. However, virtually nothing is known of
their use among ancient populations. In this paper we discuss evidence for
prebiotic use in the archaeological record from select areas of the world.
It is suggested that members of our genus Homo would have had
sufficient ecological opportunity to include prebiotic-bearing plants in
diet as early as ~ 2 million years ago, but that significant
dietary intake would not have taken place until the advent of
technological advances that characterized the Upper Paleolithic of ~40,000
years ago. Throughout human evolution, hominid populations that
diversified their diet to include prebiotic-bearing plants would have had
a selective advantage over competitors.
Introduction
Since the
1970s, there has been renewed interest between colonic function and human
health (27), with much recent attention being given to prebiotic
carbohydrates that are not available for the vertebrate digestive system
in general and for the human digestive system in particular and as such
are completely available for the abundantly present intestinal bacterial
ecosystem. Prebiotics interact in a selective way with the intestinal
ecosystem and tend to change it’s composition with potential positive
health effects for its consumer
(12, 13). The well-established ß(2-1)
fructans inulin and oligofructose continue to drive much of the current
research on the health benefits associated with prebiotics
(44, 59, 60). Although much current
research is aimed at demonstrating health benefits for modern populations,
and mechanisms for delivering them safely into the food supply
(11), very little is known about
the consumption of inulin-type fructans throughout human history.
In this paper,
we briefly review archaeological evidence for prebiotic consumption in
southern North America and select regions of the world. As a component of
human health, it is useful to consider the evolutionary role of natural
prebiotic foods from the perspective of nutritional ecology. This is
defined as the study of essential nutrient intake for the purpose of
overall human health, growth and maintenance, and general trends towards
population growth
(26, 27). In other words, a diverse
and sufficiently nutritional human diet will result in sustained or
improved human health patterns as revealed by lower infant mortality and
extension of human life expectancy.
The time-depth
afforded by archaeology is unique in that it provides a window into the
dietary and other environmental variables that have shaped our current
genetic makeup and its nutritional parameters. Significant nutritional
(agriculture) and technological
(industrial revolution) changes in
the last 10,000 years occurred too recently on a genetic time-scale for
our genome to adjust
(7, 9, 15, 63). Thus, modern
populations are selected biologically and physiologically for an
evolution-based diet that did not include many of the popular foods that
currently dominate intake. As such, the nature and composition of the
modern gut microflora is in discordance and progressively divergent from
our original, genetically determined composition.
Evolution-based Nutrition and Nutritional Ecology
Humans require
a diverse diet of nearly fifty essential nutrients for proper growth,
metabolic function and cellular repair
(25). Current nutrient requirements
and physiology have been conditioned by selective pressure and
adaptability played out on an ever changing nutritional landscape spanning
millions of years. Fossil evidence places the earliest members of our
genus
(Homo) at ~ 2 million y ago
(10, 64). Throughout much of our
history
(>99%), humans evolved on a diet
that was void of dairy foods, margarine
(separated fats), cultivated cereal
grains, and refined sugars, all of which supply as much as 60 to 70% of
the calories in many modern diets. Up until ~500 generations ago, all
humans consumed plants and animals foraged from their environment, and
consumed virtually no agricultural grains, nor processed foods. Our
evolution-based hunter-gatherer diet was high in fiber
(dietary and functional), lean
animal protein, polyunsaturated fats
(omega-3 [ω-3] fatty acids),
monosaturated fats, vitamins, minerals, phytochemicals, antioxidants, and
low in sodium
(40). Astonishingly, ‘semi-modern’
hunter-gatherers and less westernized groups that adhere more closely to
this ancient diet and lifestyle than to more westernized diets, are
largely free of chronic degenerative diseases
(7, 47) and biomarkers of illness
such as rising blood pressure, increasing adiposity, and insulin
resistance
(1, 14, 28, 29, 36, 51).
Though
traditional hunter-gatherer diet and lifestyle vanished in its ‘purest’
form in the early 20th century
(39), ongoing studies of diet and
lifestyle among less-westernized groups still remaining throughout the
world are demonstrating that models of optimal nutrition
(therapeutic diets) may be
developed from these extant evolution-based diets. Within the medical
community
(9), there is a slow but
significant movement towards acknowledging that a conceptual framework for
preventing diseases of affluence may be built upon a foundation
constructed within evolutionary theory. At the core of this theoretical
movement, often referred to as Darwinian medicine
(53, 57), is the idea that our
current genetic pool was shaped by millions of years of natural selection
in environments very different than the ones we live in today and that
much of our genetic makeup is based on a nutritional landscape that did
not include foods that currently dominate our westernized diet. The
discordance between the rapid pace of our recent
(last 10,000 yrs) cultural
adaptations
(agriculture, food processing technology)
is far outstripping our biological
(genetic) ability to keep pace.
While some
single-gene mutations
(e.g., against malaria) are
examples of the speed at which natural selection can occur, the
pathophysiology of many chronic diseases involve many more genes and much
greater periods of time to evolve
(49). While we are culturally and
socially modern, driving around in hybrid cars, we are literally and
biologically ancient hunter-gatherers.
Our modern
requirements of a great number of essential nutrients to sustain health
and well-being suggest this pattern developed early in our ancestral
history. Humans, along with other extant hominoids
(apes), evolved from a common
plant-eating ancestor some five to ten million years ago
(37). While orangutans, gorillas,
and chimpanzees have evolved on a diet mainly of fruits, leaves, flowers
and bark, humans developed a dietary path that allowed for cerebral
growth, gut anatomy, and digestive kinetics based on a mixed diet of
plants and animals. It is this diverse diet, and our ability to optimize
it through intensification and technology, that makes us unique among all
mammals.
Due to poor
preservation of food remains in the archaeological record, it is difficult
to derive exact macronutrient levels of food intake in a given diet for a
specific region. However, field studies of the few remaining
hunter-gatherer and foraging groups carried out during the early and
mid-twentieth century provide some insight into the likely range and
variability of our ancestral, evolution-based diet. In a comprehensive
review of the ethnographic data on 229 hunter-gatherer and forager groups
from all over the world, Cordain et al
(6) suggest the typical
hunter-gatherer diet derived as much as 45-65% of total energy from animal
food whenever and wherever possible, but that plant-to-animal ratios
ranged from 35:65 to 65:35, depending on environment, season, and
latitude.
Clearly, no
single diet characterizes the ‘typical or best’ hunter-gatherer, and by
extension ancestral, diet. Humans can, and do, thrive on a variety of
diets. For example, the Australian aborigines are known to have eaten some
300 different species of fruit and 150 varieties of roots and tubers
(3, 17), while Alaskan Artic
Eskimos are famous for a diet almost exclusively of raw fat and protein
from marine mammals
(20).
In the 5-7
million years since bipedal primates appeared, nearly 20 species within
the taxonomic tribe hominin have been identified in the fossil
record, with only modern Homo sapiens sapiens still standing
(10, 64). At 6 billion strong,
modern humans are clearly well-adapted and successful. Within nutritional
ecology, the physical and biological success of our species, coupled with
our genetically predetermined nutrient requirements and digestive
physiology, indicate that a diverse diet of essential nutrients
characterized much of our history. As a cornerstone of modern health and
nutrition, diverse diets are known to result in lower rates of infant
mortality and increased life expectancy
(25, 48), both of which have
significant impact of population demographics.
Support for our
diverse diet is found in the ethnographic and historical accounts among
the ‘relic’ hunter-gatherer and foraging societies discussed above. The
nutritional ecology approach suggests, due to their wide-spread occurrence
among the worlds flora and direct evidence in the archaeological record,
inulin-type fructans played an important role within a suite of essential
nutrients in long-term health and ultimate demographic success of our
species.
Prebiotics on the Archaeological Landscape
The occurrence
of the storage carbohydrate fructan in a significant portion
(>36,000 species) of the world’s
flora
(19) all but guaranteed that the
now well-studied prebiotics inulin and oligofructose were consumed by our
Pliocene and Pleistocene ancestors millions of years ago. As our early
ancestors moved from the rainforest to the parched savanna-woodlands of
subtropical Africa, subsurface tubers, rhizomes, corms, and perennial
bulbs, many rich in prebiotics, would have been a ready and important
source of energy
(18, 30). Today, many of these same
resources serve as staples for the modern foragers and farming groups
still inhabiting the same subtropical environs
(39, 61). However,
digestion-inhibiting compounds and plant toxins present in many
below-ground food sources would have limited their role as staples
in early diet of Homo until technological adaptations, such as
fire, were introduced
(42, 52). Nevertheless, as early
members of the genus Homo began their evolutionary march to
mammalian dominance, the inclusion of prebiotics within a diverse and
mixed diet would have no doubt conferred a selective advantage for the
consuming population. As the archaeological evidence reveals, prebiotics
have long been part of the human diet and in quantities for some areas and
time periods that far exceed those currently consumed by modern
populations
(58).
The physical
evidence for plant consumption by our early ancestors is virtually
nonexistent, owing to poor preservation of organic plant parts in the
archaeological records, though stable isotope analysis of skeletal remains
of early hominids are providing some insight into the quality and
diversity of early diet
(33, 43). For adequate preservation
of prebiotic food evidence in early human diet, we must travel millions of
years forward to the Upper Paleolithic
(~40,000 to 12,000 years ago) of
Western Europe and the Mediterranean Basin and to the Early Holocene
(~10,000 years ago) of North
America before significant direct and indirect evidence of prebiotic food
consumption becomes evident.
Decades of
large-scale archaeological research in North America has documented
extensive exploitation of prebiotic rich plants such as agave
(Agave spp.), sotol
(Dasylirion
spp), camas
(e.g., Camasia quamash, C. leichtlinii),
and wild onion
(Allium spp.). While a great
number of inulin-bearing plants were known as food sources among the
prehistoric and historic groups of North America
(62), these particular plants by
far provide the oldest evidence of prebiotic consumption in North America,
dating back over 9,000 years.
In the Lower
Pecos Region of the Chihuahuan Desert in west Texas along the US-Mexican
border, deeply stratified cave deposits document the use of agave, sotol,
and onion that date back nearly 9,500 years. Kept dry and preserved by the
large overhangs that characterise many of the caves and shelters of the
region, an extraordinary collection of human coprolites and preserved
macro botanical plant remains suggest that pit-baked prebiotic foods
(e.g., agave, sotol, onion) were a
mainstay of this desert economy
(50).
East of the
Lower Pecos on western edge of the Edwards Plateau in central Texas, the
deeply buried Wilson-Leonard site has produced a 2 meter diameter
rock-lined earth oven used to cook the nutritious onion-like bulbs of
camas
(Camassia spp.). Charred
camas bulbs recovered during excavation of the oven produced a date of ~
8,200 years before present
(2). Though no charred bulbs of
camas were recovered from deeper excavations, “stone-lined hearths”
underlying the camas oven were dated to ~ 9,410-9,990 years before
present, hinting at possible earlier evidence of prebiotic use.
At the
Stigewalt site in southeastern Kansas, remains of large
(> 2 m diameter), rock-filled earth
ovens with charred onion
(Allium spp.) bulbs dated ~
8,810-7,910 years before present
(55). As with the large oven at the
Wilson-Leonard site in Central Texas, the occurrence of hand-excavated
pits lined with pre-heated stones, seem to be consistently associated with
the cooking of prebiotic foods. This same pattern continues throughout the
American Southwest, where thousands of agave roasting pits
(also known as mescal pits)
are scattered about the landscape
(31). Similarly, in the American
northwest, large, rock-lined ovens were used to cook as much as 1,500 kgs
of inulin-rich camas bulbs in a single firing event
(56).
The reoccurring use of large, rock-lined earth ovens, which
are often associated with cooking of inulin-rich plants
(62), is well-documented in the
historical and ethnographic records for North America and northern Mexico.
For example, Castetter et al.
(5) describe cooking agave in pits
among the Mescalero and Chiricahua Apache of the American Southwest:
Pits in which
the crowns [agave] were baked were about ten to twelve feet in diameter
and three or four feet deep, lined with large flat rocks... Upon this, oak
and juniper wood was placed, and before the sun came up was set on fire.
By noon the fire had died down, and on these hot stones was laid moist
grass, such as bunch grass... The largest mescal crown was selected...
they threw it in and threw the other crowns after it... After the mescal [agave]
had been covered with the long leaves of bear grass and the whole with
earth to a depth sufficient to prevent steam from escaping.
In the American
Southwest, ideal surface conditions and slow rates of soil accumulation,
accompanied by repeated use of oven facilities and subsequent accumulation
of oven debris
(discarded cooking stones) over
multiple seasons, has made it possible to map thousands of cooking
facilities, which often reach over 1 meter in height and cover areas tens
of meters in diameter
(32). Synthesis of hundreds of
radiocarbon dates from cook-stone facilities across extensive areas of
southern North America
(31) has revealed a steady increase
in prebiotic food consumption beginning over 9,000 years ago, culminating
in substantial intensification around 1,250 years ago. The intensification
of prebiotic foods in southern North America
(specifically the American Southwest)
coincides with increased reliance on cultivated crops such as corn
(Zea mays), squash
(Cucurbita sp.) and beans
(Phaseolus sp.) and
large-scale growth in human population. Therefore, while populations were
making the transition to a diet heavily dependent on starchy cultivars,
prebiotic foods played an important and often increasing regional role in
a diverse nutritional economy.
As we see in
North America, the occurrence of cook-stone technology, in the absence of
recoverable plant remains, may be used as a proxy indicator to the
exploitation of prebiotic foods in the archaeological record. While a
great number of foods are known to have been processed with cook-stone,
the occurrence of large
(>1 m diameter), ovens are
consistently associated with many prebiotic foods
(31, 62).
Throughout
Western Europe, similar remains of massive cooking facilities are known to
occur in Wales, England, Scotland, Ireland, and Scandinavia. Referred to
locally as fulacht fiadh, recent urban development has led to the
excavation of a number of these mounds, which can reach over a meter in
height and several meters in diameter, representing dozens, if not
hundreds, of individual oven events. While moist ground conditions have
all but destroyed any evidence of the plants that may have been
processed in these features, radiocarbon dates on small amounts of
carbonised wood charcoal from initial heating of cook-stone indicate the
majority of mounds were constructed within the last 6,000 years. Similar
cook-stone mounds of varying sizes, dating roughly within the same time
period, are known in southern parts of Australia
(22). As seen for North America,
historical and ethnographic accounts of using large, hand-excavated pits
and heated cook-stones is noted throughout Australia. In one example,
between 1884 and 1850 British explorers observed the following among the
people at Menindee on the Darling River;
The oven is a hole dug into which are placed stones; a fire is then
made and when the stones are become sufficiently hot, whatever fibrous
things they eat, or animal, is put into this oven and covered over and a
fire made over it, when it soon gets cooked
(4).
Among the 800
plus plant foods known to have been eaten for tens of thousands of years
by Aborigines in Australia
(3), many were tuberous roots and
corms that contained prebiotic inulin
(58) and required prolonged cooking
in rock-lined pits
(16, 17, 24).
By far the
oldest known evidence of cook-stone technology
(ovens) in Europe comes from the
cave site of Abri Pataud in the Dordogne region of southern France. In
excavations by a joint American-French team between 1958 to 1964, a series
of cook-stone features, some greater than 1 meter in diameter, were dated
to ca. 33,000-18,000 years ago
(38). While it is impossible to
know if prebiotic plant tissue was processed in these ancient features, as
no direct evidence in the form of plant material was reported, their use
in cooking vegetal material is inferred from the overwhelming evidence of
similar features recorded throughout the world.
In one final
example
(56), among the more ancient
cook-stone features are those recently excavated at the on the “southern
Japanese island of Tanegashima in fine-grained tephra-rich sediments and
between lenses of well-dated volcanic ash
(8). The oldest two features are
buried 10 cm below a layer of Tane-4 volcanic ash, which is radiocarbon
dated to about 30,500 years ago. One is a sandstone lens about .75 m in
diameter and the other is a sandstone-filled basin about 1.15 x .75 m in
diameter that is underlain by carbon-stained sediment. Thermally altered
sandstone ranges in size from a few cm to 25 cm in maximum dimension.
Similar cook-stone features and fire-cracked rock scatters were found in
overlying deposits dated as late as 6500 years ago, and including several
features associated with 12,000-year-old Incipient-Jomon pottery.
Investigators concluded the Late Paleolithic cook-stone features and heavy
stone tools were indicative of a plant-based diet
(8). These cook-stone features,
especially the basin-shaped forms, closely resemble remains of earth ovens
found throughout western North America used to cook inulin-rich plant
tissue
(31)”(56).
Whereas our
ancestors consumed large amounts of inulin-containing crops, it could be
questioned whether the heat treatment by means of cook-stone ovens or
other would not destroy the inulin present in these plants. Direct tests
in conditions mimicking cook stone ovens have not been done to date. In
Louisiana and in Northern Europe inulin containing chicory roots are
roasted. The roots are spread on grids that are stacked in a particular
building. Hot air that is generated by burning wood or coal is led through
the roots, thereby heating them up to a temperature of 180°C
(356°F). It was observed that under
these conditions between 10% and 20% inulin was degraded
(41, 58). In cooking or frying
experiments with inulin containing food plants such as onions, it was show
that the losses of inulin were limited to 10% or less. From these
observations it can reasonably be concluded that the heat treatment in the
cook-stone ovens
(<100°C, products not immersed in water)
preserved the inulin content of the food plants very well, with expected
losses of less than 10%.
Discussion and Conclusion
From the
current discussion it is clear that our distant ancestors consumed, in
varying quantities, plants containing prebiotic carbohydrates. These by
definition are not digested in the upper intestinal tract and interact in
a specific way with the bacterial ecosystem which is abundantly present in
the lower intestinal tract. Consumption of prebiotic carbohydrates such as
inulin selectively promotes the growth of bacteria that are associated
with a healthy condition
(e.g. lactobacilli, bifidobacteria)
and suppress bacteria that are associated with disease
(clostridia, etc.). At the same
time the metabolic activity of the bacteria is stimulated, which results
in the production of metabolites that are absorbed in the blood and exert
beneficial effects in the rest of the body with as a direct consequence:
improved resistance to infection, better skeletal bone quality, reduced
risk for chronic diseases such as cancer, cardiovascular disease etc.
(59, 60).
The interesting
association between cook-stone technology and prebiotics offers some proxy
of initial intensification, in the absence of direct recovery of prebiotic
plant tissue. Further, the durability of many of these cook-stone features
makes their identification and possible utility in recognizing large-scale
patterns of prebiotic use across space and time feasible through inductive
principles of investigation. We suspect, that while our ancestors have
always included amounts of prebiotic plants in their diet through daily
foraging activities and that some evidence for use of cook-stone is
present during the Middle Paleolithic
(35), it was not until the onset
of the Upper Paleolithic
(~40,000 years ago), with its
ornaments, decorated tools, deliberate storage facilities, crudely
tailored clothing, art, and clear demographic pulses
(54), that prebiotic plant foods
began to play an increasing role in the dietary evolution of our species.
Increased
demographic pressure resulted in shrinking territories, making access to
preferred plants and high-return animal and aquatic resources, less
reliable. It is under this cultural pressure that initial intensification
(increased diet breadth) of under
utilized below-ground resources
(tubers, bulbs), many rich in
prebiotics, possibly took place. This form of land-use intensification
(23, 56) was the beginning of a
long-term, albeit punctuated, prebiotic revolution made possible by the
adaptation of cook-stone technology. The evolutionary implications of
prebiotic consumption on the development and relative success of our
species is unknown, and requires further research. However, advances in
processing technology, brought about during the industrial revolution in
the late nineteenth century, in conjunction with the increase in
“westernized diets” and its accompanying medical maladies, have forever
altered the delicate evolutionary-induced balance between food and human
health, thereby resetting our metabolic and genetic clocks.
The concept of
prebiotic food ingredients is an important development in nutritional
research. Beyond local effects, the idea that prebiotics can selectively
modulate gastrointestinal microbial fermentation to influence
physiological processes which are known biomarkers of potential illness
and human health is profound. However, in the case of even the
best-designed human nutrition intervention trial, optimal controls may
never be achieved, as the diet and lifestyle of – most likely all –
members will differ significantly from their evolution-based and thus
genetically determined optimal diet.
The future of
prebiotic research may be well-served with a better understanding of the
essential nutrient profiles that humans evolved on over millions of years
of selective pressure and how that relates to intestinal health, as our
evolutionary trajectory has arguably been towards maximizing our
adaptability – both physically and physiologically
(46). In other words, our
biological and physiological parameters of essential nutrients and their
conditioning of human health are, for the most part, predetermined and
grounded in our ancient past. Recent genome sequencing of
Bifidobacterium longum
(45) further points to a symbiotic
and ancient relationship between our genus and the prebiotic plants on the
landscape.
There is no
doubt that the majority of intermediate markers of disease risk and health
currently being addressed with prebiotics and modulation of the intestinal
flora have, at their source, multifactorial causes. Evolution has as a
consequence that successful living organisms do best in those environments
in which they were selected. As a consequence an informed research agenda
that includes an evolutionary perspective on ‘ancestral’ parameters of
diet and microflora composition may advance the realization and potential
of future prebiotic research with its aim of optimum health and nutrition.
Through this research agenda, it may be possible to characterize the
differences between modern and ancient intestinal health as it pertains to
microflora composition, in order to integrate microbiological,
nutritional, and epidemiological studies and data into an overarching
paradigm that can serve to establish formulations resulting in effective
recommendations for consumers.
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