Review Bioscience Microflora Vol. 25 (1), 1–8, 2006 Evolution, Nutritional Ecology and Prebiotics in Ancient Diet

Jeff D. LEACH1*, Glenn R. GIBSON2 and Jan Van LOO3

1School of Archaeology & Ancient History, University of Leicester, University Road, Leicester LE1 7RH UK and Paleobiotics Lab, 144 Arenas Valley Road, Silver City, New Mexico 88061 USA 2Food Microbial Sciences Unit, School of Food Biosciences, The University of Reading, Reading, RG6 6AP UK 3Orafti, Aandorenstraat 1, B3330 Tienen, Belgium Received for publication, October 8, 2005

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 of ~40,000 years ago. Throughout , hominid populations that diversified their diet to include prebiotic-bearing plants would have had a selective advantage over competitors. Key words: prebiotics; evolution; archaeology; nutritional ecology; cook-stone

perspective of nutritional ecology. This is defined as the INTRODUCTION study of essential nutrient intake for the purpose of Since the 1970s, there has been renewed interest overall human health, growth and maintenance, and between colonic function and human health (27), with general trends towards population growth (26, 27). In much recent attention being given to prebiotic other words, a diverse and sufficiently nutritional human carbohydrates that are not available for the vertebrate diet will result in sustained or improved human health digestive system in general and for the human digestive patterns as revealed by lower infant mortality and system in particular and as such are completely available extension of human life expectancy. for the abundantly present intestinal bacterial The time-depth afforded by archaeology is unique in ecosystem. Prebiotics interact in a selective way with that it provides a window into the dietary and other the intestinal ecosystem and tend to change it’s environmental variables that have shaped our current composition with potential positive health effects for its genetic makeup and its nutritional parameters. consumer (12, 13). The well-established β (2-1) Significant nutritional (agriculture) and technological fructans inulin and oligofructose continue to drive much (industrial revolution) changes in the last 10,000 years of the current research on the health benefits associated occurred too recently on a genetic time-scale for our with prebiotics (44, 59, 60). Although much current genome to adjust (7, 9, 15, 63). Thus, modern research is aimed at demonstrating health benefits for populations are selected biologically and physiologically modern populations, and mechanisms for delivering for an evolution-based diet that did not include many of them safely into the food supply (11), very little is the popular foods that currently dominate intake. As known about the consumption of inulin-type fructans such, the nature and composition of the modern gut throughout human history. microflora is in discordance and progressively divergent In this paper, we briefly review archaeological from our original, genetically determined composition. evidence for prebiotic consumption in southern North America and select regions of the world. As a EVOLUTION-BASED NUTRITION AND component of human health, it is useful to consider the NUTRITIONAL ECOLOGY evolutionary role of natural prebiotic foods from the require a diverse diet of nearly fifty essential nutrients for proper growth, metabolic function and *Corresponding author. Mailing address: 144 Arenas Valley Road, cellular repair (25). Current nutrient requirements and Silver City, New Mexico 88061 USA. Phone: +505-534-4065. E-mail: physiology have been conditioned by selective pressure [email protected] or [email protected]

1 2 J.D. LEACH, et al. and adaptability played out on an ever changing cars, we are literally and biologically ancient hunter- nutritional landscape spanning millions of years. Fossil gatherers. evidence places the earliest members of our genus Our modern requirements of a great number of (Homo) at ~ 2 million years ago (10, 64). Throughout essential nutrients to sustain health and well-being much of our history (>99%), humans evolved on a diet suggest this pattern developed early in our ancestral that was void of dairy foods, margarine (separated fats), history. Humans, along with other extant hominoids cultivated cereal grains, and refined sugars, all of which (apes), evolved from a common plant-eating ancestor supply as much as 60 to 70% of the calories in many some five to ten million years ago (37). While modern diets. Up until ~500 generations ago, all humans orangutans, gorillas, and chimpanzees have evolved on a consumed plants and animals foraged from their diet mainly of fruits, leaves, flowers and bark, humans environment, and consumed virtually no agricultural developed a dietary path that allowed for cerebral grains, nor processed foods. Our evolution-based growth, gut anatomy, and digestive kinetics based on a hunter-gatherer diet was high in fiber (dietary and mixed diet of plants and animals. It is this diverse diet, functional), lean animal protein, polyunsaturated fats and our ability to optimize it through intensification and (omega-3 [ω-3] fatty acids), monosaturated fats, technology, that makes us unique among all mammals. vitamins, minerals, phytochemicals, antioxidants, and Due to poor preservation of food remains in the low in sodium (40). Astonishingly, ‘semi-modern’ archaeological record, it is difficult to derive exact hunter-gatherers and less westernized groups that adhere macronutrient levels of food intake in a given diet for a more closely to this ancient diet and lifestyle than to specific region. However, field studies of the few more westernized diets, are largely free of chronic remaining hunter-gatherer and foraging groups carried degenerative diseases (7, 47) and biomarkers of illness out during the early and mid-20th century provide some such as rising blood pressure, increasing adiposity, and insight into the likely range and variability of our insulin resistance (1, 14, 28, 29, 36, 51). ancestral, evolution-based diet. In a comprehensive Though traditional hunter-gatherer diet and lifestyle review of the ethnographic data on 229 hunter-gatherer vanished in its ‘purest’ form in the early 20th century and forager groups from all over the world, Cordain et al. (39), ongoing studies of diet and lifestyle among less- (6) suggest the typical hunter-gatherer diet derived as westernized groups still remaining throughout the world much as 45–65% of total energy from animal food are demonstrating that models of optimal nutrition whenever and wherever possible, but that plant-to- (therapeutic diets) may be developed from these extant animal ratios ranged from 35:65 to 65:35, depending on evolution-based diets. Within the medical community environment, season, and latitude. (9), there is a slow but significant movement towards Clearly, no single diet characterizes the ‘typical or acknowledging that a conceptual framework for best’ hunter-gatherer, and by extension ancestral, diet. preventing diseases of affluence may be built upon a Humans can, and do, thrive on a variety of diets. For foundation constructed within evolutionary theory. At example, the Australian aborigines are known to have the core of this theoretical movement, often referred to as eaten some 300 different species of fruit and 150 Darwinian medicine (53, 57), is the idea that our current varieties of roots and tubers (3, 17), while Alaskan Artic genetic pool was shaped by millions of years of natural Eskimos are famous for a diet almost exclusively of raw selection in environments very different than the ones we fat and protein from marine mammals (20). live in today and that much of our genetic makeup is In the 5–7 million years since bipedal primates based on a nutritional landscape that did not include appeared, nearly 20 species within the taxonomic tribe foods that currently dominate our westernized diet. The hominin have been identified in the fossil record, with discordance between the rapid pace of our recent (last only modern Homo sapiens sapiens still standing (10, 10,000 years) cultural adaptations (agriculture, food 64). At 6 billion strong, modern humans are clearly well- processing technology) is far outstripping our biological adapted and successful. Within nutritional ecology, the (genetic) ability to keep pace. physical and biological success of our species, coupled While some single-gene mutations (e.g., against with our genetically predetermined nutrient requirements malaria) are examples of the speed at which natural and digestive physiology, indicate that a diverse diet of selection can occur, the pathophysiology of many essential nutrients characterized much of our history. As chronic diseases involve many more genes and much a cornerstone of modern health and nutrition, diverse greater periods of time to evolve (49). While we are diets are known to result in lower rates of infant mortality culturally and socially modern, driving around in hybrid and increased life expectancy (25, 48), both of which PREBIOTICS IN ANCIENT DIET 3 have significant impact of population demographics. prebiotic food consumption becomes evident. Support for our diverse diet is found in the Decades of large-scale archaeological research in ethnographic and historical accounts among the ‘relic’ North America has documented extensive exploitation of hunter-gatherer and foraging societies discussed above. prebiotic rich plants such as agave (Agave spp.), sotol The nutritional ecology approach suggests, due to their (Dasylirion spp), camas (e.g., Camasia quamash, C. wide-spread occurrence among the worlds flora and leichtlinii), and wild onion (Allium spp.). While a great direct evidence in the archaeological record, inulin-type number of inulin-bearing plants were known as food fructans played an important role within a suite of sources among the prehistoric and historic groups of essential nutrients in long-term health and ultimate North America (62), these particular plants by far demographic success of our species. provide the oldest evidence of prebiotic consumption in North America, dating back over 9,000 years. PREBIOTICS ON THE ARCHAEOLOGICAL In the Lower Pecos Region of the Chihuahuan Desert LANDSCAPE in west Texas along the US-Mexican border, deeply The occurrence of the storage carbohydrate fructan in stratified deposits document the use of agave, sotol, a significant portion (>36,000 species) of the world’s and onion that date back nearly 9,500 years. Kept dry flora (19) all but guaranteed that the now well-studied and preserved by the large overhangs that characterise prebiotics inulin and oligofructose were consumed by many of the and shelters of the region, an our Pliocene and ancestors millions of years extraordinary collection of human coprolites and ago. As our early ancestors moved from the rainforest to preserved macro botanical plant remains suggest that pit- the parched savanna-woodlands of subtropical Africa, baked prebiotic foods (e.g., agave, sotol, onion) were a subsurface tubers, rhizomes, corms, and perennial bulbs, mainstay of this desert economy (50). many rich in prebiotics, would have been a ready and East of the Lower Pecos on western edge of the important source of energy (18, 30). Today, many of Edwards Plateau in central Texas, the deeply buried these same resources serve as staples for the modern Wilson-Leonard site has produced a 2 m diameter rock- foragers and farming groups still inhabiting the same lined used to cook the nutritious onion-like subtropical environs (39, 61). However, digestion- bulbs of camas (Camassia spp.). Charred camas bulbs inhibiting compounds and plant toxins present in many recovered during excavation of the oven produced a date below-ground food sources would have limited their role of ~ 8,200 years before present (2). Though no charred as staples in early diet of Homo until technological bulbs of camas were recovered from deeper excavations, adaptations, such as fire, were introduced (42, 52). “stone-lined ” underlying the camas oven were Nevertheless, as early members of the genus Homo dated to ~ 9,410-9,990 years before present, hinting at began their evolutionary march to mammalian possible earlier evidence of prebiotic use. dominance, the inclusion of prebiotics within a diverse At the Stigewalt site in southeastern Kansas, remains and mixed diet would have no doubt conferred a selective of large (> 2 m diameter), rock-filled earth ovens with advantage for the consuming population. As the charred onion (Allium spp.) bulbs dated ~ 8,810–7,910 archaeological evidence reveals, prebiotics have long years before present (55). As with the large oven at the been part of the human diet and in quantities for some Wilson-Leonard site in Central Texas, the occurrence of areas and time periods that far exceed those currently hand-excavated pits lined with pre-heated stones, seem consumed by modern populations (58). to be consistently associated with the of The physical evidence for plant consumption by our prebiotic foods. This same pattern continues throughout early ancestors is virtually nonexistent, owing to poor the American Southwest, where thousands of agave preservation of organic plant parts in the archaeological roasting pits (also known as mescal pits) are scattered records, though stable isotope analysis of skeletal about the landscape (31). Similarly, in the American remains of early hominids are providing some insight northwest, large, rock-lined ovens were used to cook as into the quality and diversity of early diet (33, 43). For much as 1,500 kg of inulin-rich camas bulbs in a single adequate preservation of prebiotic food evidence in early firing event (56). human diet, we must travel millions of years forward to The reoccurring use of large, rock-lined earth ovens, the (~40,000 to 12,000 years ago) of which are often associated with cooking of inulin-rich Western Europe and the Mediterranean Basin and to the plants (62), is well-documented in the historical and Early (~10,000 years ago) of North America ethnographic records for North America and northern before significant direct and indirect evidence of Mexico. For example, Castetter et al. (5) describe 4 J.D. LEACH, et al. cooking agave in pits among the Mescalero and to the excavation of a number of these mounds, which Chiricahua Apache of the American Southwest: can reach over a meter in height and several meters in diameter, representing dozens, if not hundreds, of Pits in which the crowns [agave] were individual oven events. While moist ground conditions baked were about ten to twelve feet in have all but destroyed any evidence of the plants that may diameter and three or four feet deep, lined have been processed in these features, radiocarbon dates with large flat rocks… Upon this, oak and on small amounts of carbonised wood charcoal from juniper wood was placed, and before the sun initial heating of cook-stone indicate the majority of came up was set on fire. By noon the fire had mounds were constructed within the last 6,000 years. died down, and on these hot stones was laid Similar cook-stone mounds of varying sizes, dating moist grass, such as bunch grass… The roughly within the same time period, are known in largest mescal crown was selected… they southern parts of Australia (22). As seen for North threw it in and threw the other crowns after America, historical and ethnographic accounts of using it… After the mescal [agave] had been large, hand-excavated pits and heated cook-stones is covered with the long leaves of bear grass and noted throughout Australia. In one example, between the whole with earth to a depth sufficient to 1884 and 1850 British explorers observed the following prevent steam from escaping. among the people at Menindee on the Darling River; In the American Southwest, ideal surface conditions The oven is a hole dug into which are and slow rates of soil accumulation, accompanied by placed stones; a fire is then made and when repeated use of oven facilities and subsequent the stones are become sufficiently hot, accumulation of oven debris (discarded cooking stones) whatever fibrous things they eat, or animal, is over multiple seasons, has made it possible to map put into this oven and covered over and a fire thousands of cooking facilities, which often reach over 1 made over it, when it soon gets cooked (4). m in height and cover areas tens of meters in diameter (32). Synthesis of hundreds of radiocarbon dates from Among the 800 plus plant foods known to have been cook-stone facilities across extensive areas of southern eaten for tens of thousands of years by Aborigines in North America (31) has revealed a steady increase in Australia (3), many were tuberous roots and corms that prebiotic food consumption beginning over 9,000 years contained prebiotic inulin (58) and required prolonged ago, culminating in substantial intensification around cooking in rock-lined pits (16, 17, 24). 1,250 years ago. The intensification of prebiotic foods in By far the oldest known evidence of cook-stone southern North America (specifically the American technology (ovens) in Europe comes from the cave site of Southwest) coincides with increased reliance on Abri Pataud in the Dordogne region of southern France. cultivated crops such as corn (Zea mays), squash In excavations by a joint American-French team between (Cucurbita sp.) and beans (Phaseolus sp.) and large-scale 1958 to 1964, a series of cook-stone features, some growth in human population. Therefore, while greater than 1 m in diameter, were dated to ca. 33,000– populations were making the transition to a diet heavily 18,000 years ago (38). While it is impossible to know if dependent on starchy cultivars, prebiotic foods played an prebiotic plant tissue was processed in these ancient important and often increasing regional role in a diverse features, as no direct evidence in the form of plant nutritional economy. material was reported, their use in cooking vegetal As we see in North America, the occurrence of cook- material is inferred from the overwhelming evidence of stone technology, in the absence of recoverable plant similar features recorded throughout the world. remains, may be used as a proxy indicator to the In one final example (56), among the more ancient exploitation of prebiotic foods in the archaeological cook-stone features are those recently excavated at the on record. While a great number of foods are known to have the “southern Japanese island of Tanegashima in fine- been processed with cook-stone, the occurrence of large grained tephra-rich sediments and between lenses of (>1 m diameter), ovens are consistently associated with well-dated volcanic ash (8). The oldest two features are many prebiotic foods (31, 62). buried 10 cm below a layer of Tane-4 volcanic ash, Throughout Western Europe, similar remains of which is radiocarbon dated to about 30,500 years ago. massive cooking facilities are known to occur in Wales, One is a sandstone lens about 0.75 m in diameter and the England, Scotland, Ireland, and Scandinavia. Referred to other is a sandstone-filled basin about 1.15 × 0.75 m in locally as fulacht fiadh, recent urban development has led diameter that is underlain by carbon-stained sediment. PREBIOTICS IN ANCIENT DIET 5

Thermally altered sandstone ranges in size from a few cm etc. (59, 60). to 25 cm in maximum dimension. Similar cook-stone The interesting association between cook-stone features and fire-cracked rock scatters were found in technology and prebiotics offers some proxy of initial overlying deposits dated as late as 6,500 years ago, and intensification, in the absence of direct recovery of including several features associated with 12,000-year- prebiotic plant tissue. Further, the durability of many of old Incipient-Jomon . Investigators concluded the these cook-stone features makes their identification and Late Paleolithic cook-stone features and heavy stone possible utility in recognizing large-scale patterns of were indicative of a plant-based diet (8). These prebiotic use across space and time feasible through cook-stone features, especially the basin-shaped forms, inductive principles of investigation. We suspect, that closely resemble remains of earth ovens found while our ancestors have always included amounts of throughout western North America used to cook inulin- prebiotic plants in their diet through daily foraging rich plant tissue (31)” (56). activities and that some evidence for use of cook-stone is Whereas our ancestors consumed large amounts of present during the Middle Paleolithic (35), it was not inulin-containing crops, it could be questioned whether until the onset of the Upper Paleolithic (~40,000 years the heat treatment by means of cook-stone ovens or other ago), with its ornaments, decorated tools, deliberate would not destroy the inulin present in these plants. storage facilities, crudely tailored clothing, art, and clear Direct tests in conditions mimicking cook stone ovens demographic pulses (54), that prebiotic plant foods have not been done to date. In Louisiana and in Northern began to play an increasing role in the dietary evolution Europe inulin containing chicory roots are roasted. The of our species. roots are spread on grids that are stacked in a particular Increased demographic pressure resulted in shrinking building. Hot air that is generated by burning wood or territories, making access to preferred plants and high- coal is led through the roots, thereby heating them up to a return animal and aquatic resources, less reliable. It is temperature of 180°C (356°F). It was observed that under this cultural pressure that initial intensification under these conditions between 10% and 20% inulin was (increased diet breadth) of under utilized below-ground degraded (41, 58). In cooking or frying experiments with resources (tubers, bulbs), many rich in prebiotics, inulin containing food plants such as onions, it was show possibly took place. This form of land-use that the losses of inulin were limited to 10% or less. intensification (23, 56) was the beginning of a long-term, From these observations it can reasonably be concluded albeit punctuated, prebiotic revolution made possible by that the heat treatment in the cook-stone ovens (<100°C, the adaptation of cook-stone technology. The products not immersed in water) preserved the inulin evolutionary implications of prebiotic consumption on content of the food plants very well, with expected losses the development and relative success of our species is of less than 10%. unknown, and requires further research. However, advances in processing technology, brought about during DISCUSSION AND CONCLUSION the industrial revolution in the late 19th century, in From the current discussion it is clear that our distant conjunction with the increase in “westernized diets” and ancestors consumed, in varying quantities, plants its accompanying medical maladies, have forever altered containing prebiotic carbohydrates. These by definition the delicate evolutionary-induced balance between food are not digested in the upper intestinal tract and interact and human health, thereby resetting our metabolic and in a specific way with the bacterial ecosystem which is genetic clocks. abundantly present in the lower intestinal tract. The concept of prebiotic food ingredients is an Consumption of prebiotic carbohydrates such as inulin important development in nutritional research. Beyond selectively promotes the growth of bacteria that are local effects, the idea that prebiotics can selectively associated with a healthy condition (e.g. lactobacilli, modulate gastrointestinal microbial fermentation to bifidobacteria) and suppress bacteria that are associated influence physiological processes which are known with disease (clostridia, etc.). At the same time the biomarkers of potential illness and human health is metabolic activity of the bacteria is stimulated, which profound. However, in the case of even the best- results in the production of metabolites that are absorbed designed human nutrition intervention trial, optimal in the blood and exert beneficial effects in the rest of the controls may never be achieved, as the diet and lifestyle body with as a direct consequence: improved resistance of – most likely all – members will differ significantly to infection, better skeletal bone quality, reduced risk for from their evolution-based and thus genetically chronic diseases such as cancer, cardiovascular disease determined optimal diet. 6 J.D. LEACH, et al.

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