Preserving Microbial Diversity

In November 2011 we spent a week among the bushmen of Botswana and Namibia collecting stool samples to characterize the impact of varying diets on the microbiota.

De Filippo C et al. PNAS 2010 Aug 17;107(33):14691-6
Arumugam M et al. Nature, May 12;473(7346):174-80

Even though this data does not measure actual consumption, that’s done by the good folks over at the National Health and Nutrition Examination Surveys, and the data is alarming.

According to the economists at the ERS, the “average” American (all age groups) consumed 2,594 calories in 2009. As the graph below illustrates, 619 (24%) of those calories came from flour and cereal products (wheat, rice corn, etc.), 596 (23%) from added fats, oil, and dairy fats (butter, margarine, lard, salad and cooking oils, half and half, etc), and so on. Perhaps most striking is the so few calories in the average American diet that are derived from vegetables and fruit.

A mere 87 (3%) calories a day for fruits and 118 (5%) calories from vegetables. We all know that many fruits and veggies are predominately water, but 87 calories from fruits?! Really? If my math is correct – and to put it into perspective – 87 calories of fruit is equivalent to 8-9 McDonald’s French fries.

Of the veggies consumed, a whopping 47% were potatoes (e.g., chips, french fries). Other movers in the veggie category included carrots, onions, beans, legumes, cucumbers, and sweet corn – but all were in the single digits.

Below is a graph plotting the caloric consumption for each of our categories over the past 40 years (calories plotted on left axis). Despite the never-ending messaging to consume more fruits and veggies from every nutritional corner on earth, and the government’s “eat 5 servings of fruits and vegetables” initiatives (think 5 A Day program, which is now 5-9 servings a day), fruit and vegetable consumption has remained more or less flat. However, we have seen a steady rise – and even some striking spikes – in other categories.

Interestingly, the government-sponsored 5 A Day program, which was founded in 1991 by the National Cancer Institute and the National Institutes of Health, was farmed out a few years ago to the Produce for Better Health Foundation, which relies on support from private industry to get out their Fruits & Veggies More Matters message.

As calculated by the ERS researchers, the average daily calories from fruits and veggies above translate into 0.9 servings a day of fruit and 1.7 servings a day for vegetables, for a total of 2.6 servings a day. Even doubling that number to reach the minimum recommended 5 servings a day, something that has not been possible in nearly 40 years, would also mean doubling production. Doubling, much less tripling produce production in the U.S., is much harder than it sounds and likely means more imports – something that freaks out the food safety folks given the soaring land prices in the U.S. (i.e., all the good arable land is taken up with existing crops, cows or pavement).

This is why the launch of the USDA’s new MyPlate, and Harvard’s dueling Healthy Eating Plate, are not likely to get average Americans to consume more fruits and veggies. The messaging is the same, so the results will not be any better (history is our guide here). To honestly increase produce consumption to reasonable levels – what ever that is – will require significant policy initiatives/changes from the top down. We will need to go beyond a poorly funded MyPlate program and overhaul the system fencerow to fencerow and all the way to the grocery isle and classrooms of America. That means farm subsidies, looking at predatory marketing by food companies, addressing social inequalities from WIC to grocery stores in disadvantaged neighborhoods, better planned communities, and dare I say, teaching underlying biological principles of human evolution and genetics that are selected for our current nutritional needs.

Unfeigned biologically-driven education + policy is what will move the needle.

Billed as no ordinary weeklong survival course, Cody’s Desert Drifter is designed to “strip you of everything you thought you needed in the wilderness.” And in my case, that also meant missing the fine print on the course paperwork I filled out to join this wandering band that would have allowed me a small bag of GORP (granola, oats, raisins, and peanuts) to tide me over as we chased crickets and rabbits for food in northern Arizona. Hunger set in early for me.

As hungry as I was in those first days of calorie burning hikes in extreme temperatures and rough terrain, and an all night march in near freezing temps (shivering burns a large amount of calories), I was faintly comforted by the knowledge that the progressive effects of heat and hypothermia were more likely to kill me than my hunger pangs. With no blankets and a strict “no fire” rule in those first few days, I was left to snippets of communal body heat when we kind of slept and what nourishment I could forage from a landscape that moved quickly under our feet. We were a tribe of nine, drifting now, and the do more with less mantra of the Aboriginal Living Skills School, founded by our barefooted leader, began to sink in.

After 48 hours of one extreme survival scenario after another and no sleep, I really began appreciating fine print as my body sucked energy stored from my adipose tissue (aka body fat) and began sipping my strategic energy reserves of glycogen from my liver. My system was struggling to feed my brain and its ability to execute the simplest of cognitive tasks – like putting one foot in front of the other, and completing Cody’s primitive skills modules, which also required the dual survival skill of channeling my ancestors with one side of my starved brain and calling up my genetically coded ability to complete fine motor skills with the other. Just another day in the life of our ancient genome, but a rude awakening to a system accustomed to quick energy inputs from a modern nutritional landscape dotted with Chipotle’s and 24-hour Circle K’s.

The course was designed to beat you down, and beat you down it did. But the one thing that helped me through those first few days – and the remainder of the weeklong survival course for that matter – was my understanding of the ancient bioreactor deep in my gut. Nearly five feet in length, the human colon and its trillions of resident bacteria have the ability to generate calories from almost any plant matter no matter how nutrient-poor that matter may be.

Like the fermentation that takes place in the various stomach chambers of cows, goats etc., the gut bacteria breaks down undigested plant material through various processes and produce byproducts such as short chain fatty acids, which are then absorbed into the body and utilized by the muscles and organs as energy. Depending on the type of undigested plant material (e.g., resistant starch, cellulose, hemicelluloses, inulin, pectins [aka dietary fiber]), the gut bacteria can convert 1 gram of plant matter into as much as 1 to 1.5 calories. Not bad when you consider the straight-up digestible carbohydrates available, say, in a slice of bread, converts as 1 gram ingested to 4 calories. In other words, bacteria are the reason horses, cows, deer and similar critters can extract enough calories from blades of grass.

So throughout those first few days I literally grazed as we whisked along, grabbing handfuls of green grass, wild flowers, not so tasty berries, and anything that I could choke down. These handfuls of green matter were broken down by my commensal bacteria and turned into calories. Though it was difficult to calculate, I probably generated 300-400 much-needed calories a day from my new trail diet (but likely burned 6-10,000 calories a day). In order to generate even a modest 1,500 to 2,000 calories from the trail diet, I would have had to literally chew all day, and probably locate more energy dense plants (e.g., root foods) that also contained some straight up carbohydrates and starches. We did eventually eat our way into some nutritious stands of cattails – once Cody allowed us the comfort of fire days into the Desert Drifting to cook them.As with other plant eaters, our early ancestors relied on gut bioreactors to extract calories from otherwise undigested foods. While our colons make up a smaller percentage of our overall gut system today, our ancestors relied on the colonic bioreactor to generate calories from twigs, leaves, flowering plant parts and so on – similar to our tree swinging cousins. But as the quality of our diet improved – through technology and ultimately the advent of fire – the requirement of our bioreactor decreased and therefore its overall size. Even though our colons and their bioreactor function remain a significant part of our gut systems, our modern diet hardly delivers the fermentation products down the pipe as it once did – as I experienced during my week of foraging across the landscape. And there-in lies possibly the biggest unappreciated health crisis facing our modern society today.

With a reduction in the consumption of undigested plant parts – to say nothing of the reduction in diversity of plants – we have literally stopped using the calorie-generating bioreactors handed down to us by our ancestors, and in the process created an imbalance in our microbiota that evolved within our gut ecosystem. By not receiving a steady supply and diversity of plant parts (again, fiber), the bacteria living in our guts cannot do their evolutionary job and fight off invading pathogens by increasing acidity, and therefore compete for nutrients and niches in order to flourish along the colonic wall.

The existence of residential microbiota is ancient, providing evidence of the co-evolution of bacteria and animals. In the case of humans, we are endowed with a “specific” set of bacteria at birth and our life history pushes and pulls that balance on a daily basis. Though there is poorly defined variation among human populations, there exists a genome-specific set of players that are significantly influenced by diet.

Rapid changes in diet in our post-modern era are predictably producing different diseases. In short, changes in human ecology equals changes in our microbiota. Add to this the astonishing increases in Caesarean sections that limit perinatal transfer of maternal microflora, which is further confounded by the replacement of mother’s milks with formula – which creates an imbalance in natural, indigenous flora.

Advances in molecular and genomic techniques confirm the role of infection in an increasing number of acute and chronic diseases, made more likely by diet and lifestyle-induced imbalance. Disease was heavy on my mind as I drug my weakened body from one cattle tank to another to scoop stagnant, muddied and often dead animal-laden water. But unlike my GORP-eating fine-print-reading colleagues, my steady but limited diet of grass blades and flowers meant my microbiota was bolstered for anything that may have slipped past the iodine drops.

While the biggest threat I faced was diarrhea from bad water, I wouldn’t have experienced the impact for a day – or even longer – as I wouldn’t have experienced any symptoms at the time of consumption. In fact, the connection between “dirty” water and diarrhea was not made until the 1800s. This same delay from infection to symptom is what delayed acceptance of infectious causation of other vector-borne diseases such as malaria – transmitted by mosquitoes.

But what if many of the chronic diseases plaguing us today, like heart disease, breast cancer, colon cancer, diabetes and Alzheimer’s, all in fact could be ascribed to infectious causation? What if these terrible diseases had a more acute phase, would we then recognize them as the result of infection? Is the lag time between infection and manifestation that characterizes a particular chronic disease shifting our medical attention away from the obvious? I think medical professionals who ignore infectious causation of many of the big chronic killers today will look as myopic to medical historians in 20-30 years from now as the researchers who dismissed infectious causation for pneumonia, chicken pox, and diarrhea did not that long ago.

As we rounded out our desert drifter week we did finally get to enjoy some freshly gathered crawfish from the Verde River along with some crispy grasshoppers roasted on a stick. This was made all the more enjoyable by the fact that I, and everything I ate, was covered in dirt teaming with natural microorganisms that my ancestors had long ago forged a symbiotic relationship with. Dirt is good. Cody, you the man. I never felt so alive. Peace.

Modern technology has condensed some of our ancient nutritional landscape into tightly spaced plastic bins and bowls sitting atop crunchy ice. A tidy landscape of such nutrition would have made the toughest of our ancestors weep. And what do most of us do upon stepping up to this diverse bounty? Flinch! And begin filling a clamshell container with piles of a single leafy green and maybe a pinch of this and that.

Over the last few months I have stalked the salad bar — I know, creepy — at my local grocery store and witnessed firsthand well-intentioned folks filling their salad container with water-laden leafy greens and not much else. If we channeled our ancestors for just a moment, we would fill this finite container with less leafy greens and a spoonful of every plant you can stand to eat. If it’s ten plants, then ten it is. If it’s fifteen, then even better.

Building a better salad means diversity. No single plant contains everything you nutritionally need; it’s the combination of physical (think fiber) and chemical (vitamins and minerals) diversity that is more in line with the edible landscape that selected the nutritional requirements of our modern genome.

A greater diversity of plants in your container will likely reduce the water percentage by weight — making you feel fuller, longer. The diversity of this mixed meal will slow down digestion and absorption, also contributing to feeling fuller for longer.

Importantly, each plant at your local salad bar contains a different physio-chemical structure of dietary fiber. With each bite of this diversity, you will more naturally stimulate the growth of good-for-you bacteria living deep in the self-contained ecosystem known as your gut. Yes, good for-you-bacteria break down and grow on dietary fiber — and the more diverse, the better. So try this next time you fill a container at your local grocery store and see how you feel.

And remember, nothing in nutrition makes sense unless in the light of evolution, friendos. Don’t flinch.

As Bittman and so many others suggest, investing in the problem now may save us trillions downstream. Seems simple enough. But the trillion-dollar question is, of course, where best to spend our energy and resources if such an effort was “really and honestly” undertaken by government and industry. Bittman and others obviously and rightly argue that altering lifestyle choices is the best and most affordable means to attenuate the problem. But the combat-diet-related-diseases-by-changing-my-diet drumbeat at the behest of the food police predictably makes the general public flinch. And too often behavioral modification, when served up government style, misses the point all together – such as the notion that posting calorie info on menu boards in 20% of the eateries in America will actually have a meaningful impact (click here for our two-cents on posting caloric info).

It’s simple enough to continue morally shouting from the rafters that disease prevention through lifestyle modification is a better long-term strategy than treatment of disease and costs through legislatively mandated improvement of the bureaucracy of the health care delivery system from bed pans to pill companies. Until we come to the realization that mind-jarring paradigm shifts are needed to honestly and cost effectively address the issues, insurance companies will continue dancing on our graves.

The first big shift will need to be the role of government in research priorities. In our current system, our tax dollars go towards funding profitable treatments for private companies, rather than investing in research that makes people healthier and cheaper. If the long-term outlook of rising costs are as dire as they appear, it would make sense, at least on the research investment side of the equation, to aggressively treat illness in the short term so as to make the overall investment more profitable in the long term. In other words, it should be the role of government to fund good things that are not profitable as it should be obvious that private business is poorly suited to address such things as prevention given the inherent conflict of interest — whether its stated or not. Said differently, funded research that makes people healthy cheaply, instead of making people healthy profitably, reveals that prevention rather than treatment should be the desire of government.

If we are going put some of our eggs in the prevention basket, then we will need a massive investment in education, as our current understanding of what a healthier lifestyle looks like is colored by myths, half truths, and the interests of the same free market entities we so like beating up on the treatment side. It’s not much of a stretch to suggest that we are poorly equipped as a nation of people, when it comes to truly understanding our own biological past and the role of diet in our health and well-being, may in fact be a bigger hurdle than the more headline-grabbing rants against the health care system and government meddling. This is unfortunately well-illustrated in a recent Facebook poll we conducted asking the question, “Do we have millions of diabetics in America because we don’t eat organic foods?”

Even though there is zero connection between diabetes and organically grown foods, 26% of the 517 respondents think that there is and a full 21% are not sure. (Click here for our take on organic foods and the science). In other words, 46% of the respondents think organic foods do or “might” have some causal role in diabetes. The fact that a nutritional fetish such as organic and similar fantasies has replaced reason in our understanding of what causes disease, and thus how to exercise meaningful lifestyle prevention, positions us as the proverbial sitting duck. A cynical person may think this is where they want us — in the cross hairs. Either way, that is where we are — uninformed about biological sciences and evolutionary processes. A nutritional opiate for the masses. Stupidity.

It’s not enough to create nanny states and industries that suggest we should just prevent by changing our lifestyle. We must first agree on how we define health and well-being, and then initiate sweeping reform and begin re-educating our nation about the biological realities that underpin our unique species. Fortunately, many of the most interesting and useful answers are coded in our genes and our evolutionary past if we are brave enough to look there.

Archaeological research in the northern Tucson Basin over the last two decades has confirmed that species of the genus Agave were cultivated in extensive agricultural fields marked by the presence of rock piles, terraces, and check dams. Researchers estimate that ~ 10,000 agaves were harvested annually from a standing population of greater than 100,000 cultivated plants in the larger fields, potentially providing the annual caloric requirements for as many as 155 persons. However, the annual caloric return from harvested agave has been overestimated by ~55% when you consider that inulin-type fructans are the major storage carbohydrate in agave. As a nondigestible carbohydrate, inulin and its subgroup oligofructose are not absorbed in the small intestine, but are fermented in the large bowel and thus have a lower net energy value than traditional carbohydrates such as starch.

Introduction

Over 300 species of agave have been reported throughout the American Southwest and northern Mexico (Gentry 1982). Early travelers and ethnographers in the region noted the importance of agave and other desert succulents as a food source among indigenous populations (e.g., Castetter et al. 1938), while ongoing archaeological research throughout the southern US continues to expand our knowledge of the importance and antiquity of agave exploitation (e.g., Dering 1999; Fish et al. 1982, 1985; Leach 2005; Leach and Lopez, in press). Perhaps one of the more fascinating and important aspects of this research has been the identification of agave as cultivated plant among the desert Hohokam of southern Arizona (Fish et al. 1982, 1985). Along the mountains slopes and bajadas of the lowlands north of Tucson, extensive fields of rock piles and stone borders, along with charred remains of agave plant remains in rock-lined roasting pits, confirm the importance of agave in a mixed economy among these desert farmers.

This paper reports that the caloric yields from agave harvested from these extensive fields have been overestimated as a result of not considering the type of carbohydrate stored in agave plants. When the appropriate conversion factors are applied to the carbohydrate portion of the plant tissue, the overall calories derived from a given amount of agave is reduced by more than half, thus reducing the contribution of cultivated agave in the subsistence economy for inhabitants of this semi-arid region.

The Non Digestible Carbohydrates Inulin and Oligofructose in Agave

The three principal reserve carbohydrates in plants are starch, fructan, and sucrose, with fructan being present as the major storage carbohydrate in at least 36,000 species of plants (Hendry 1987). Agaves utilize crassulacean acid metabolism (CAM) for CO₂ fixation and fructans are the principal photosynthetic products generated (Wang and Nobel 1998; Leach and Lopez, in press; Lopez et al. 2003).

From a chemical point of view, fructans can be divided into inulin, levan, phlein, graminan, and kestoses based on their respective fructosyl-fructose linkage structure. Of interest here is the fructan inulin and its subgroup oligofructose. Inulin is a polydisperse set of predominately linear molecules made up of D-fructose residues linked to a terminal glucose residue by β(2→1) osidic bond (Van Loo et al. 1995). The degree of polymerization (DP) of inulin varies between three and sixty-five (Van Loo 2004). Oligofructose is a subgroup of inulin, consisting of polymers with a DP ≤10. While the fructan structure may vary within the genus Agave, inulin-type fructans are the most predominant (Leach and Lopez in press; Lopez et al. 2003).

The unique linkage between the fructose molecules of inulin and oligofructose distinguish them from typical carbohydrates in that they resist digestion by human alimentary enzymes and absorption in the small intestine but are hydrolyzed and fermented by colonic microflora (Roberfroid 1993). This fermentation produces gases (H₂, CO₂, CH₄) and short chain fatty acids, such as butyrate, that are subsequently absorbed and utilized for energy. The intestinal physiological effects demonstrated by the carbohydrates inulin and oligofructose therefore meet the basic and essential definition of a dietary fiber (Cherbut 2002; Roberfroid 1993, 2004), and thus a net energy content lower than digested carbohydrates such as starch.

Energy Contribution of the Nondigestible Carbohydrate Fraction of Agave

As a non digestible dietary fiber, inulin and oligofructose are the major storage carbohydrate in the genus Agave and should be treated differently than traditional carbohydrates when calculating caloric yield. To estimate the calories from a given amount of food, internationally accepted conversion factors for the protein, fat and carbohydrate present in a given food item are utilized. In the US, the Atwater factor (Atwater 1910) is typically utilized. Traditionally, the energy value of foods is given in kilocalories (kcal), a unit of heat, as measured by the amount of heat obtained by burning any food in a calorimeter (Livesey et al. 2000). In a mixed food diet energy is calculated by chemically analyzing the amount of protein, fat, and carbohydrates present, then multiplying those amounts by appropriate energy conversion factors –  “the average amounts of energy provided to the body by 1 g of typical food fat, protein or carbohydrate (Livesey et al. 2000).

When calculating energy contribution by the Atwater factor, all fats provide 9 kcal per gram, protein provides 4 kcal per gram, and all carbohydrates provide 4 kcal per gram. These ‘catch-all’ conversion factors for energy contribution of protein, fat and carbohydrates are applied by archaeologosts, anthropologists, and ethno-botanists when calculating the potential kcal yield of a given plant resource to the overall diet and when ranking resources for the purposes of optimal foraging models (e.g, Dering 1999). However, advances in food science, as demonstrated by in vitro and in vivo studies (Livesey et al. 2000), demonstrate that the declared caloric contribution of a food item such as a carbohydrate, and the scientifically determined energy value, may differ, depending on the type of carbohydrate and its linkage structure.

Of interest here is the conversion factor of 4 kcal g for all carbohydrates. As already mentioned, the fructans  inulin and oligofructose present in the genus Agave are non digestible dietary fiber, not subject to hydrolysis and absorption in the small intestine. Research conducted in the realm of food science, specifically on inulin and oligofructose derived from chicory (Cichorium intybus), have demonstrated that the selective anaerobic hydrolysis and fermentation of these substrates produces short-chain fatty acids (acetate, propionate, butyrate) and lactic acids that are subsequently absorbed by the cells to produce energy, thus salvaging a portion of the originally ingested food ingredient (for an extensive review see Roberfroid 1993). Therefore, their contribution to the metabolic energy of the host is reduced and indirect (Roberfroid 1999: 1436S), and the conversion factor of 1.5 kcal g, rather than the ‘catch-all’ of 4 kcal g, should be utilized in determining caloric yield from the carbohydrate portion of the genus Agave.

Discussion

Researchers working in the Tucson Basin estimate that within a well-studied five square kilometer area along a series of bajadas, project as many as 42,000 rockpiles and 120,000 meters of terraces and checkdams were utilized for the cultivation of agave (Fish et al. 1985). Based on these data, the researchers estimate that as many 102,000 agave plants could have been grown at one time, producing an annual harvest of 10,200 plants. With an approximate weight of 4 kilograms per agave heart, the annual yield would result in 40.8 metric tons of edible agave. Citing nutritional data by Ross (1944), the researchers further suggest that agave provides 347 calories per 100 grams, potentially providing the annual caloric requirements of 155 persons.

From the nutritional data cited by Fish et al (1985) it is not clear what conversion factors were used to estimate the 347 calories per 100 g of edible agave. It is safe to assume that given the 1944 date for the source of the nutritional data, that a conversion factor of 4 kcal g for the carbohydrate portion was utilized. Working east of the Tucson Basin, Dering (1999: Table 3) provides recent nutritional analysis of pit baked samples of Agave lechuguilla. The nutritional composition (adjusted for dry weight) of 100 g sample is as follows: 6.18 g protein, 3.5 g fat, and 65.6 g carbohydrates. The calculated caloric value of cooked agave is thus the following:

6.18 g protein x 4 kcal/g + 3.5 g fat x 9 kcal/g + 65.6 g carbohydrate x 1.5 kcal/g = 154.62 kcal/100 g

On the basis of the nutritional data from Agave lechuguilla, adjusted for the conversion factor of 1.5 kcal / g for non digestible carbohydrates, the caloric contribution of agave harvested from the extensive fields in the Tucson Basin are reduced by ~ 55% from 347 calories per 100 g to 154.62 calories per 100 g. The original estimate that the annual caloric requirements of 155 persons were potentially met by the harvested agave is accordingly reduced to ~ 70 persons.

Further, Fish et al (1985:112) suggest that “agave hearts of small Southwestern species approximate four kilograms,” but do not specify if this is harvested and uncooked plants, or plants that have been harvested, cooked, and dried to reduce spoilage. This variable is critical as the scale of the agricultural fields and the size of the roasting pits recorded among the fields suggest that large quantities of agave were processed. This bulk processing of agave in the roasting pits was no doubt followed by pounding (kneading) of the cooked agave into cakes or loaves that were subsequently air-dried for transport and possible storage (Note the reduction of water via air-drying reduces the chance of spoilage). This final stage of processing is consistent with ethnographic observations of agave processing (Ferg 2003), and greatly reduces the water content and weight of the processed plant tissue, thus the potential annual caloric yield of the fields.

In his study of the small species Agave lechuguilla, Dering (1999: Table 5) reports an average cooked and dried weight of 0.086 kilograms per agave heart, which is well below the 4 kilograms per agave heart reported by Fish et al. (1995:112). In a series of unpublished experimental studies with Agave murpheyi, a candidate species that may have been cultivated in the agricultural fields of the Tucson Basin (Fish et al. 1982, 1985), this author found that cooked and air-dried agave hearts (n=7) weighed on average about 1.2 kilograms. While this is higher than reported for the smaller species studied by Dering, it is considerably less than that reported by Fish et al (1985). If we assume that the 4 kilogram per harvested agave heart cited by Fish et al(1985:112) is for uncooked and undried agave, and subsistitute the 1.2 kilograms per cooked and air-dried agave arrived at through the experimental studies, then the annual yield of agave from the large fields is reduced from 40.8 metric tons to 12.24 metric tons, accordingly.

The overall reduction in annual yield calculated for cooked and subsequently dried agave estimated from experimental study, coupled with the calories per 100 g sample adjusted for the conversion factor for non digestible carbohydrates, suggest the annual caloric requirements of less than two dozen persons would have been met with an annual harvest of 10,200 plants.

Conclusion

The identification of agave as a cultivated crop in southern Arizona is a significant contribution to our understanding of human adaptation and paleonutrition in this semi-arid region. The presence of inulin and oligofructose as the dominant carbohydrate stored in the genus Agaveallows for refinement in the net energy contribution of this plant. The adjusted energy yield of agave has resulted, along with the adjusted cooked and dried weight of agave hearts, in an overall reduction in potential caloric contribution of agave to the diet and economy of these desert farmers.

The following discussion raises the question of why so much effort (labor) was invested in the cultivation of agave, when one realizes the low caloric yields from such agricultural practices and the additional labor required to harvest, cook, and dry the plant tissue for transport and possible storage. Clearly, the inclusion of cultivated agave in the diet by these desert farmers serves as a reminder as to the difficulties of subsisting in a semi-arid region, where ever increasing demographic pressure and unpredictable environmental realities required cultivation of such marginal resources an unavoidable necessity.
References

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Castetter, E.F., W.H. Bell, and A.R. Grove. 1938. The early utilization and distribution of Agave in the American Southwest. Biological Series 5(4). Bulletin 335, University of New Mexico Press, Albuquerque.

Cherbut, C. 2002. Inulin and oligofructose in the dietary fibre concept. British Journal of Nutrition 87: S59-S162.

Dering, P. 1999. Earth-Oven Plant Processing in Archaic period Economies: An Example from a Semi-Arid Savannah in South-Central North America. American Antiquity 64(4): 659-674.

Ferg, A. 2003. Traditional Western Apache Mescal Gathering is Recorded by Historical Photographs and Museum Collections. Desert Plants 19(2).

Fish, S.K., P.R. Fish, and J. Madsen. 1992. The Marana Community in the Hohokam World.Anthropological Papers of the University of Arizona 56. University of Arizona Press, Tucson.

Fish, S.K., P.R. Fish, C. Miksicek, and J. Madsen. 1985. Prehistoric Agave Cultivation in Southern Arizona. Desert Plants 7(2): 107-112, 100.

Gentry, H.S. 1982. Agaves of Continental North America. University of Arizona Press, Tucson.

Hendry, G. 1987. The ecological significance of fructan in a contemporary flora. New Phytologist, Suppliment 106: 201-216.

Leach, J.D. 2005. Sharp Increase in Cook-Stone Use in the Chihuahuan Desert During Periods of Agricultural Intensification.

Leach, J.D. and M.G. López . In Press. Prebiotic Inulin and Oligofructose from Agaves and Their Role in Prehistoric Diet: An Example from the Chihuahuan Desert. The Texas Journal of Science.

Livesey, G., D. Buss, P. Cousement, D.G. Edwards, J. Howlett, D.A. Jonas, J.E. Kleiner, D. Müller, A. Sentko. 2000. Suitability of traditional energy values for novel foods and food ingredients. Food Control 11: 249-289.

Lopez, M.G., N.A. Mancilla-Margalli, and G. Mendoza-Diaz. 2003. Molecular Structures of Fructans from Agave tequilana Weber var. azul. Journal of Agricultural and Food Chemistry 51: 7835-7840.

Roberfroid, M. 1993. Dietary fiber, inulin and oligofructose: a review comparing their physiological effects. Critical Review of Food Science and Nutrition 33: 103-148.

Roberfroid, M. 1999. Caloric Value of Inulin and Oligofructose. Journal Nutrition 129: 1436S-1437S.

Ross, W. 1944. The present day dietary habits of the Papago Indians. M.S. thesis. University of Arizona, Tucson.

Van Loo, J. 2004. The specificity of the interaction with intestinal bacterial fermentation by prebiotics determines their physiological efficacy. Nutritional Research Reviews 17: 89-98.

Van Loo, J., P. Coussement, L. De Leenheer, H. Hoebregs, and G. Smits. 1995. On the presence of inulin and oligofructose as natural ingredients in the Western diet. Critical Review of Food Science and Nutrition 35: 525-552

Wang, N. and P. Nobel. 1998. Phloem transport of fructans in the crassulacean acid metabolism species Agave deserti. Plant Physiology 11: 709-714.

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 20^th 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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Being sustainable and going green are all the rage these days – and for good reason. The ground swell around these often-overused words has been gaining for decades, due in large part to the hard work of many, the public outcry to outrageous denials and policies of a recent few, and a little film starring some guy named Al. Spurred by threats of petrodictators and the moral imperative that meeting the needs of the present without compromising the ability of future generations to meet their own needs, never have so many wanted to do so much.

Though the outcome and impact of our environmental and social awakening is unknowable at the moment, one thing is for sure – people are paying attention, and they get it. If so many can grasp the complexity of environmental issues and chart a collective way forward, it lends hope to the possibility that the same enthusiasm and understanding can be built around the quagmire that is human health. The problems are legion and all to familiar: two of every three adults in the US are overweight or obese, 20 million people have diabetes, our joints and guts ache, our arteries are clogged, hypertension is common, Alzheimer’s is on the rise, as are autism, asthma, and we are popping more pills than any generation in human history. Americans are sick people. And what’s our national (and Louisiana) plan to deal with these epidemics? Streamline the record keeping!

As with any disaster, there is an evidence trail – a chain of events. Planes just don’t fall from the sky; it starts with one bird, then another. Likewise, diabetes does not appear out of the blue; it’s the metabolic expression of a chain of events, as is the case with most chronic disease. But more specifically, it’s a nutritional chain of events. Our national obsession with global warming and undoing our dependence on fossil fuels provides an interesting analogy for a way to think about human health and disease. At the core of both are energy choices and the side effects of those choices.

Human energy choices (calories), like hydrocarbon energy sources (oil, gas, coal), have some expected and unintended consequences. As our economy gorges itself on petro-calories, we are causing irreparable damage to the environment (e.g., strip mining, oil spills) and creating byproducts (carbon dioxide) that further the length in a chain of events (e.g., global warming) on our way to some unknown disaster that is sure to occur at some point in the future (e.g., rising oceans, mass species extinctions, wars, famine, the reemergence of Richard Simmons). Depending on your threshold for social, physical, and economic pain, anyone of these links in the chain events could be your disaster. The same works for human health and disease.

At the sake of overusing the analogy, global warming just doesn’t appear one day for no apparent reason; it’s the result of a chain of events – some natural and some not. The natural cadence of the earths recurring gravitational cycles coupled with fluctuations in the amount of incoming solar radiation have plunged the earth in and out of ice ages for eons. In other words, global warming is genetically-geologically-cosmologically programmed into the earths DNA. At the heart of the sustainability discussion is the role of humanities energy choices is causing global warming to express itself in an unnatural way – that is, just a little too warm due to unnatural inputs (carbon dioxide from excess burning of hydrocarbons).

It can be suggested that the foods we eat – by proxy the energy choices we make in the form of calories – are equally as unsustainable to the human body as the societal and environmental impact of our reliance on crude oil has been, if measured by the increasing links in the chain of metabolic events of human disease. For example, in the development of type 2 diabetes, metabolic imbalances of elevated glucose and subsequent insulin levels caused from an unsustainable intake of energy in the form of highly processed and easily digested and absorbed carbohydrates – made more complicated by increasing insulin resistance – are links in a chain of events that began with energy choices. Depending on your level of pain and definition of disaster, selecting a link in the chain of events as “the” disaster of being a type 2 diabetic may range from amputation of an appendage, complications leading to heart attack or stroke, or financial hardship. Insulin is to diabetes what green house gases are to global warming: a byproduct of unsustainable energy choices that can lead to disastrous outcomes.

Suggesting that the metabolic disorder of type 2 diabetes is somehow “in your genes” would be like blaming global warming as solely a natural cycle preordained within the earth’s DNA. Though earth’s metaphorical DNA provides the opportunity for global surface temperatures to rise to levels sufficient to generate other links in our chain of environment events, it’s our lifestyle of dependence on fossil fuels that triggered the environmental chain of events in the same way our lifestyle choices and our lack of understanding of fuel needs of the human body represent any early link in the chain of events we know as type 2 diabetes. Seen in this way, type 2 diabetes is a sustainability issue and must be approached in a similar manner as global warming: a radical shift in where and how we get energy – or else. Kicking the metabolic can down the road and medicating the problem has been the strategy of our modern healthcare system, with the lip service towards prevention (altering energy types and quantities) serving as some kind of professional, industry, and governmental cover. The similarities to the long, and tired history of fossil fuels, global warming, and industry and governmental inaction is striking.

Interestingly, aside from exploring alternative energy sources like wind, air, solar, and hydrothermal, much of our current and future efforts are targeted at “true” biofuel: those created by the fermentation of plant matter by microorganisms. In short, varying species of bacteria can break down the complex physical and chemical structure of fiber in things like grass into smaller molecules that can be “essentially eaten” by other strains of bacteria that produce various byproducts that can be captured and used as energy to fuel our industrious modern lifestyle. As an alternative source of energy, this proposed organic and symbiotic relationship with microbes, whereby we provide them with a steady supply of nutrients to grow and multiply and they provide us with byproducts we then harvest for energy for a healthier sustainable future, is exactly what happens in the human body when we utilize those same plant resources. Or at least what used to happen.

The human body is home to trillions of fiber-fermenting bacteria: always has been, always will be. Like the massive vats and slimy-green tubes scientists and engineers are erecting to generate energy from industrious microbes, our own biofuel reactor is the last five feet or so of our gastrointestinal tract – the colon. Large spans of evolutionary time have selected for certain groups of bacteria that would inhabit the human body in a symbiotic way – the initial founding population we receive today is from our mother’s after moving through the birth canal. Similar to the symbiotic relationship between engineers and energy-generating microbes, our long march to mammalian dominance included a similar relationship: we provide certain members of the outside world a warm, safe place to live (colon) and a steady supply of fermentable nutrients (fiber from plants), they in return extract energy (calories) from those plants for us with ingenious mechanisms we did not need to evolve ourselves.

Not that long ago, humans relied heavily on our own bioreactors to generate upwards of 10 to 15% of our energy needs.[i] Today, given our low-intake of dietary fiber this number has dropped well into the low single digits. Our evolutionary-determined dependence on our bioreactors for fuel was no accident, it evolved over long periods of time, selecting for a certain set of bacteria to keep it all in balance. This means humans have two sources of energy to fuel our active lives: one from carbs+proteins+fats digested and absorbed in the small intestine and calories generated from short chain fatty acids created as a byproduct of the fermentation of undigested plant material (fiber). This makes our own body the first and most efficient hybrid fuel system of humanity. Sorry Toyota. However, things are going terribly wrong.

The modern food chain looks nothing like the nutritional landscape upon which we evolved this symbiotic bioreactor. In essence, much of our design (our physiology) is built on this hybrid fuel system – in the same way clever automobile engineers design systems around the understanding that fuel will come from two sources (in the case of some hybrid cars, one combustible engine and the other electrically charged batteries). If your hybrid car – or human body – is built around these basic energy and design elements, then any misuse or nonuse of one of the fuel systems will result in a negative impact to the broader system – i.e., the damn thing just starts falling apart. In the case of the human body, we are generating too much energy on the front end from excess highly processed carbohydrates that are easily digested and absorbed, and too few calories (energy) are being generated from the bioreactor. The imbalance causes elevated levels of insulin to deal with the excess glucose from the carbs and the insulin in turn is having some devastating effects, the least of which is its ability to interfere with fat metabolism (contributing ‘significantly’ to weight gain).

Even worse in the unsustainable fuel environment created by our modern diet is its impact on the microbial factory workers deep in our bioreactors. By not keeping the bioreactor fed, we are disrupting the delicate balance among our intestinal microflora. This unsustainable disturbance is causing some basic housekeeping problems within the bioreactor. A well-fed bioreactor is critical to maintaining the delicate mucosal barrier (think mucus) lining our intestinal tract which, when unattended by chemical and physical interaction by a balanced intestinal flora from a fully functional bioreactor, will get out of whack. We know this as inflammation and various symptoms related to irritable bowel disease and some intestinal cancers. Medicating this problem rather than feeding the bioreactor and its inhabitants is like resolving our dependence on oil by increasing fuel mileage of cars – while useful at some level, does not address the original link in the chain of events.

In short, pick your chronic disease (disaster) and you can trace it back to unsustainable energy choices, the human hybrid bioreactor, and an imbalance with our microbial friends – collectively known as the microbiome. This is why the National Institutes of Health recently launched the Human Microbiome Project and dozens upon dozens of peer-reviewed articles are published every month on the role of intestinal microflora in human health and disease. This is also why there are major efforts underway within the pharmaceutical industry to develop drugs targeted at gut bugs and why researchers in cancer, diabetes, heart disease, and so on are pointing their collective molecular and genetic tools in the direction of the bioreactor to glean understanding of the role of microbes in their respective fields. Medical science and nutrition is undergoing a revolution of sorts with the realization that the human body is a superorganism, composed of an amalgam of microbial and H. sapiens cells, where the survival of microbe and human is interdependent.

But you would not know this if you scanned the bio’s of the 13 experts recently selected by the US Departments of Agriculture and Health and Human Services (this is the department Tom Daschle was bumped from running) to review the latest medical and nutrition science for the purposes of updating the Dietary Guidelines for Americans and accompanying Food Pyramid for 2010, as not one of the experts selected to tell us what to eat to maintain optimal health and prevent disease has a background in microbiology or ever conducted basic research on the effects of diet on microbiome health. This means we will get yet another set of dietary guidelines that ignores the basic biological fact that 90% of the cells in the human body are not even human, but microbial.

It wasn’t until it sunk in that our national obsession with petro-calories had impacts well beyond our geographical borders and high into our atmosphere, did we start to address the significant social and political changes necessary to halt and potentially reverse this unsustainable and deeply immoral behavior. The state of the healthcare in the US has probably reached that point as well, though we don’t think about the issue as a moral imperative owned by society in total, rather we point fingers at individual behavior. By several measures, health care spending continues to rise at a rapid rate. In 2008, total national health expenditures were expected to rise 6.9 percent – two times the rate of inflation.[ii] Total spending was $2.4 trillion in 2007, or $7900 per person, representing 17 percent of the gross domestic product (GDP). US healthcare spending is expected to increase at similar levels for the next decade reaching $4.3 trillion in 2017, or 20 percent of GDP.

You don’t need to be an economist to see the problem: this is not sustainable – not if you want to fund basic services, education, R&D, and so on. Something will have to give. Experts agree that our health care system is riddled with inefficiencies, excessive administrative expenses, inflated prices, poor management, and inappropriate care, waste and fraud – all of which increase the cost of medical care and health insurance for employers and workers and affect the security of families. While “streamlining the system” is needed, it’s the nutritional equivalent of “Drill, Baby, Drill!.” While it’s politically expedient and seems at face value to be a reasonable approach, it’s shortsighted and potentially devastatingly naïve. All the while our next economic tsunami in the form of rising healthcare costs is building on the horizon with universal healthcare serving as the sea bottoms earthquake trigger.

While we should embrace comprehensive healthcare for all citizens, any large-scale strategy that does not include owning up to or being able to pay for our unsustainable reliance on highly processed and easily digested and absorbed energy sources and its negative impact on the efficiency and time-honored role of our human bioreactor and its inhabitants to human health and disease, will only come up short. The food industry is to human health what oil companies are to global warming. Some tough decisions will have to be made that will affect a variety of industries in the food chain from plough to plate – the question is whether we want to the industries or us to suffer.

As healthcare costs rise, as a percentage of the pubic purse, no longer do our individual dietary choices impact just “us” and our families – they affect us all. No longer can the food and pharmaceutical industries just say they are simply filling a need and no longer can the government stand idly by. Though our culture and social differences define us, the simple economics of our democracy link us in a way that makes the sheer mass of our unsustainable energy (calorie) choices and its impact on health and disease a moral imperative at least on par with that of global warming. It is, after all, a link in that chain as well.

[i] Note that addition to undigested plant matter that reaches the colon and thus fermented, cells that “fluff off” our intestinal wall, some resistant starches, and undigested sugar alcohol and protein is also fermented in the human bioreactor.

[ii] Keehan, S. et al. “Health Spending Projections Through 2017, Health Affairs Web Exclusive W146: 21 February 2008.

Archaeological evidence from dry cave deposits in the northern Chihuahuan Desert reveal intensive utilization of desert plants that store prebiotic inulin-type fructans as the primary carbohydrate. In this semi-arid region limited rainfall and poor soil conditions prevented the adoption of agriculture and thus provides a unique glimpse into a pure hunter-forager economy spanning over 10,000 years. Ancient cooking features, stable carbon isotope analysis of human skeletons, and well-preserved coprolites and macrobotanical remains reveal a plant-based diet that included a dietary intake of ~135 g/d of prebiotic inulin-type fructans by the average adult male hunter-forager. These data reveal humans are well adapted to daily intakes of prebiotics well above those currently consumed in modern diet or administered in current medical studies.

Introduction

Advances in molecular microbiology continue to further our understanding of the role of intestinal microbiota in modulating aspects of our postnatal development, adult physiology and overall health and well being^(1-3). Throughout human evolution, microbial growth via hydrolysis and fermentation of undigested exogenous carbohydrates has been critical to maintaining the dynamic ecological equilibrium between predominantly obligate anaerobes (e.g., Bacteroides, Lactobacillus, Bifidobacterium, Clostridium, Escherichia), various yeasts and other microorganisms in the colon⁽⁴⁾. Though poorly understood, our so-called “westernized” diet⁽⁵⁾, which is dominated by easily digested carbohydrates, may be influencing host-microbe symbiosis through a quantitative reduction in the physical and chemical diversity of undigested carbohydrates^(6-8).

Since it was discovered that mammalian digestive enzymes could not hydrolyse b–glucosidic bonds found in some carbohydrates, such as inulin-type fructans⁽⁹⁾, these oligosaccharides and polysaccharides have emerged as prebiotics; able to escape metabolism in the upper intestine and selectively stimulate the growth and metabolic activity of beneficial bacteria (e.g., bifidobacteria and lactobacilli), while suppressing the growth of less desirable microorganisms⁽¹⁰⁾. The (re)equilibration of our westernized guts through the prebiotic effect can result in a wide range of physiological benefits to the host, including reduced gut infections, improved lipid metabolism, improved mineral absorption, enhanced immuno-modulation, and reduced risk of carcinogenesis⁽¹¹⁾. However, initial faecel microflora composition, dosage and duration of dosage, as well as the physio-chemical structure of the substrate, can have measurable outcome on the prebiotic effect^(12-14).

Current daily intake of prebiotic fructo-oligosaccharides in the USA is 1-4 g, and 3-11 g in western Europe⁽¹⁵⁾. Prebiotics are formulated into an increasing number of foods and embraced by dieticians⁽¹⁶⁾, but little is known about dietary intake of prebiotic carbohydrates by ancestral populations. Said differently, were prebiotics part of the nutritional landscape upon which our organic human-microbiota symbiosis was selected? While prebiotic plant foods have been available throughout human evolution, advances in technology has increased consumption within the last 40,000 years^{(7, 17)}. Unique archaeological preservation in the arid regions of the Chihuahuan Desert provide a glimpse into dietary intake of prebiotics that far exceed those consumed by modern humans.

Prehistoric Diet of the Chihuahuan Desert

In the semi-arid northern Chihuahuan Desert, near the modern town of Del Rio, Texas, archaeological research over the last four decades has revealed an extraordinary well-preserved prehistoric record dating back over 10,000 years⁽¹⁸⁾. Erosion and down cutting of the limestone canyons and plateaus have created numerous overhangs, rock shelters, and caves of stratified layers of faunal and botanical remains, human skeletons and mummies, archaeological cooking features and an unparalleled collection of desiccated human feces (coprolites) in deposits often meters deep. Though rainfall was limited, three rivers in the area provided a water supply that supported a diversity of plants and wildlife.

Detailed paleodietary studies^(19-23) demonstrate these prehistoric populations consumed a wide variety of plants, animals and other resources including prickly pear, agave, mesquite, sotol, acorns, walnut, berries, pecan, acacia, onion and other geophytes, rodents, turtle, fish, rabbits, hares, insects, birds, reptiles, and deer. Analysis of well preserved faunal and macrobotanical remains from excavated rock shelters and caves reveals a broad-spectrum diet of wild plants and predominately small animals for the entire 10,000-year record. Among the consumed plants, the desert succulents Agave lechuguilla(agave), Dasylirion sp. (sotol), and Opuntia sp. (prickly pear) were heavily utilized, along with Allium drummondii (onion), Yucca sp. (yucca), and Prosopis sp. (mesquite). No evidence of agriculture is present in the area, owing to limited rainfall, high evaporation rates, and poor soil conditions.

Of particular interest are agave, sotol, and onion, all three of which store inulin-type fructans as the major carbohydrate^{(15, 24-25)}. The epidermal tissue (hearts) of agave and sotol were harvested in large quantities and processed in rock-lined earth ovens heated with fuel wood and cooked for >40.00 h. The cooked material is eaten immediately, or pounded into sheets, dried and stored for later consumption⁽²⁶⁾. The moist cooking environment of the earth oven reduces their toxicity and improves the nutritional profile⁽²⁷⁾. Evidence of these massive cooking facilities dot the arid landscape and the remains (leaf bases, fragments) of agave and sotol are well-represented in cultural layers in caves throughout the region⁽²⁶⁾. Wild onion was cooked and eaten, but also consumed raw.

Stable carbon isotope analysis on skeletal material recovered from various deposits in the area suggested that 45 to 68 percent of the diet may have been derived from C⁴ and CAM plants, with CAM plants (e.g., agave) making the greater contribution⁽²⁸⁾. Plants with Crassulacean acid metabolism (CAM) photosynthetic pathways leave distinct ¹³C signatures in the tissues of the animals that consume them.

Analysis of 359 human coprolites dating throughout the 10,000 year sequence from various cave deposits support the wide-spread consumption of agave, sotol, and onion, as undigested fragments and DNA remnants of these plants are identified from these well preserved samples⁽²⁹⁾.

Available evidence (macrobotanical, cooking features, stable carbon isotopes, coprolites) across multiple excavated rock shelter and cave sites suggest that agave, sotol and onion were dietary staples with agave and sotol contributing significantly more calories. These data suggest that 60 to 80 percent of the calories were provided from plant resources. For this paper, it will be assumed that only 50 percent of the diet (carbohydrate + protein + fat) was derived from plants and that conservatively 20 percent of the calories from this plant portion of the diet was derived from the carbohydrate portion(fructan) of agave, sotol, and onion. The fructan fraction (dry matter) of agave and sotol is between 65 to 70 percent (dry weight) and 41 to 88 percent for onion^{(15, 26)}. All three plants were available throughout the year and agave and sotol can be considered the primary carbohydrate source in the diet. Note that yucca and prickly pear were also heavily utilized and contain small amounts of inulin-type fructans, but will not be considered in the following discussion.

If it is assumed that an adult male hunter-forager from this desert population consumed on average 11,297 kj/d (2,700 kcal)⁽³⁰⁾, then 5,648 kj/d (1,300 kcal) were derived from plants and of that, the three fructan plants contributed 1,130 kj/d (270 kcal). The much larger size of agave and sotol, and overall abundance on the landscape, compared to the small bulbs of wild onion from the region (Allium Drummondii Regel.), along with the archaeological evidence, suggests that agave and sotol may have collectively contributed up to 80 to 90 percent of the inulin-type fructans in the diet.

The fructans in agave and sotol consist of a linear and linear and branched mixture of β(2→1) andβ(2→6) linkages with a DP range of 3-32^(24-25). Agave and sotol fructans have been categorized as graminans and branched neo-fructans⁽²⁵⁾. The prebiotic effect of species of agave and sotol has recently been demonstrated⁽³¹⁾. Species of modern onions have a lower molecular weight of ~DP3-10⁽³²⁾.

As mentioned, agave and sotol were cooked in earth ovens for >40.00 h prior to consumption. The cooking of these desert succulents is supported by the presence of massive accumulations of thermally altered stones known as burned rock middens, some measuring 5 to 20 meters in diameter, representing hundreds of cooking events per facility. Experimental data suggest that while the initial heating of the stones within the earth ovens reached temperatures of 300⁰C, the food “packages” only achieved peak temperatures ranging from 90⁰C to 106⁰C for a portion of the entire cooking period⁽³³⁾.Temperatures of 100⁰C have been shown to degrade inulin ~7-10 percent^(34-35).

The degradation of inulin-type fructans is critical, as heat creates lower molecular weight fractions (mono- and disaccharides) and breaks the beta bonds that make the fructan unavailable to enzymatic hydrolysis in the upper gastrointestinal tract. Once degraded and the b–glycosidic bonds were broken, the carbohydrate is digested and absorbed in the small intestine and unavailable for microbial fermentation and therefore do not contribute to the prebiotic effect. For the purpose of this paper, the degradation of 25 percent will be assumed for pit baked fructans, more than double the published rate.

Of the 1,130 kj/d (270 kcal) contributed by agave, sotol, and onion, 283 kj (68 kcal)(25%) would have been provided by the degraded fructans at a rate of 16.74 kj/ g (4kcal/g), following standard conversion rates for digested carbohydrates⁽³⁶⁾. However, since selective anaerobic hydrolysis and fermentation is necessary to salvage calories from undigested fructans, an energy contribution of 6.28 kj/g (1.5 kcal/g) is applied for those byproducts utilized by the host for energy⁽³⁷⁾. Therefore, the remaining 847 kj (202 kcal) not provided by the degraded fructans would be contributed by 135 g/d of prebiotic inulin-type fructans.

Concluding Remarks

Well-preserved archaeological remains from the northern Chihuahuan Desert reveal prehistoric populations relied heavily on desert plants that store inulin-type fructans for over 10,000 years. Evidence for the intensive use of these prebiotic plants is provided by extant cooking features, macrobotanical evidence, stable carbon isotope analysis of human remains, and preserved human coprolites.

Conservative estimates of the contribution of inulin-bearing plants in the diet suggest that the average male hunter-forager from this population would have consumed ~135 g/d of prebiotics, and adult females ~108 g/d (based on ~20% fewer calories). The absolute dietary intake of prebiotic inulin-type fructans would have no doubt fluctuated from day-to-day and season-to-season, but does illustrate the highest reported intake of any prehistoric or modern population in the literature.

When the non starch polysaccharides (e.g., cellulose, hemicelluose, lignin) from agave, sotol, onion, and the other dozens of plants from the diet is considered, the overall dietary intake of fibre all sources ranges from ~150 to 225 g/d for an adult male. Further, when all fermentable substrates, such as non-starch polysaccharides, resistant starch, unabsorbed sugars, dietary protein, gut secretions, mucus, sloughed epithelial cells entering the large intestine⁽³⁸⁾ on a daily basis are considered, a significantly greater portion of basal energy needs are provided from the large intestine for this prehistoric population than are observed among modern, westernized populations. The greater energy contribution from undigested carbohydrates would result, along with the minimally processed diet in general for this prehistoric population, in less need for the hormone insulin to be secreted. This is a desirable outcome as rates of obesity and diabetes increase in our modern world.

Even as the ~135 g/d is difficult to comprehend in the context of our modern diet, its also useful to remember that the total dietary fiber component for this prehistoric population, as with most ancestral groups⁽³⁹⁾, was characterized by an extraordinary diversity of fibre sources that were linear and branched and low and high molecular weights. This is the nutritional landscape upon which our genome and symbiotically evolved microbiome were selected.

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For well over 100 years, researchers have known that germs live within, on, and often travel through the human body via our intestinal tract on a daily basis and as such, play a role in many acute and chronic diseases plaguing humanity. It has only been within the last decade that significant advances in molecular techniques have revealed the delicate symbiotic relationship we share with trillions of bacteria in our gut and their role in early and ongoing immune and gut development, defense against pathogens, and harvesting and absorption of important nutrients and calories from foods we consume.

So important is the relationship we share with our microbial hitchhikers that experts consider their collective mass (>1 kg) deep in our bowels as a metabolic organ just as important to well being as a healthy liver, heart, or pancreas. Without these microbes, our lives would be impossible. For this reason, the absence of expertise in microbial ecology and evolution as it pertains to human health and disease is striking. A quick search on PubMed, an on-line database of articles from medical journals maintained by The National Library of Medicine, produces thousands of articles published within the last decade that demonstrate the role of gut microbes in diseases ranging from diabetes, heart disease, cancer, asthma, obesity, osteoporosis, irritable bowel disease and a range of other autoimmune and inflammatory diseases. In other words, a significant portion of ailments Americans suffer from – and often die because of – have an intimate connection to the health and well-being of our gut bugs.

As newborns, we enter this world sterile but are quickly populated by microbes as we pass through the microbe-rich birth canal. Within the first few hours and days of life, microbes passed to us by mother – and a few others from our new surroundings – begin populating our gastrointestinal tract, with the largest number residing in our colon. Throughout life, these first colonizers perform their evolutionary job of keeping us safe from invading pathogens and aid in the development and maintenance of our immunity. However, they require nutrients to maintain a balance of good vs bad bugs in a daily battle of germ warfare.

Early in life, this nutrient base is derived from undigested substances in mother’s milk. However, as we age and start consuming food, dietary fiber and resistant starch in our plant foods serve as the nutrients our gut bugs need to thrive and do their evolutionary job of keeping us healthy. As long as we provide them a safe, warm and nutrient-rich environment, all is well. But our so-called westernized diet which is dominated by highly processed carbohydrates (processed grains, added sugars) has shifted the nutrient base just enough to effect the balance of our gut bugs. With the average American consuming less than 15 grams a day of dietary fiber from a very limited number of sources, we have, along with our wide-scale abuse of antibiotics that impact our healthy bacteria as well, started a large-scale experiment that is assuredly part of the health problems facing us today.

What we don’t need is another set of dietary guidelines that only consider the health of our single human genome, and ignores the health of the trillions of other genomes that make up our superorganism. A superorganism approach would consider the mountains of new science and would honestly address the biological and ecological reality of the nutritional landscape that selected our current nutritional parameters and the nutritional symbiosis that must be maintained between “us” and “them.” We need dietary guidelines that promote an emphasis on the diversity of nutrients (fiber and resistant starch, specifically) that our gut bugs need and in quantities (40 to 80 grams a day) that more closely mimic our shared evolutionary past.

The realization that human health and disease is significantly linked to dietary inputs and that by altering those inputs to increase the diversity and quantity of dietary fiber and resistant starch in diet can have positive effects on the health of gut bugs and thus us, should not be ignored. Developing new dietary guidelines for our nation without considering the human-microbe relationship in health and disease would be a folly.

As of August 22, 2008, the Food and Drug and Administration (FDA) will allow food processors to irradiate iceberg lettuce and fresh spinach for the purpose of zapping E. coli and other pathogens. This ruling has been some time in the making and was recently fast-tracked due to the high profile spinach outbreak of 2006 and the pesky Salmonella Saintpaul outbreak of 2008. The FDA’s 42-page ruling, which you can read here, predictably has consumer groups howling. Standard complaints and concerns run the gamut from “irradiation reduces the nutritional value of food, creates molecules unknown in nature, and changes the taste, color, and firmness of some veggies,” to “irradiating veggies is just plain creepy.”

The idea behind irradiation is simple: kill bugs. People in the produce industry call this a kill step. When you cook meat or boil veggies in your home you practice your own kill step, as microbes are pretty much terminated by temperatures above 140 degrees or so.

The Centers for Disease Control and Prevention (CDC) states that a little over 208,000 people a day suffer from some level of food poisoning resulting in diarrhea, cramping, and vomiting. Of these, roughly 5,000 die from complications associated with foodborne pathogens each and every year in the U.S. While many blame sloppy farming practices and poor government oversight for these numbers, our westernized diet of highly processed carbohydrates and low fiber intake may be more to blame.

In either case, consumers are losing confidence in the produce industry’s ability to keep bad bugs out of fresh produce, and the industry views irradiation as the future of marketing ‘bug-free’ products to bolster consumer confidence. The consumer anxiety created by the high profile Salmonella Saintpaul outbreak of 2008, along with lobbyist-led efforts to change the law that requires food that has been irradiated to be labeled with the radura label and carry the words “irradiated”, replacing it with the much nicer sounding “cold pasteurized,” is all but guaranteeing widespread adoption of irradiation – which will no doubt be promoted by government-backed consumer education programs in the years ahead with your tax dollars.

As fresh produce loses its innocence as it enters the irradiation era, nobody, including the FDA, USDA, or CDC, is asking what appears to be an obvious question: do we really want to kill ‘all’ the bugs on our produce? An eerily similar question was posed in 1945 by British bacteriologist Alexander Fleming, who discovered the antibiotic penicillin, when he warned in an interview with the New York Times that misuse of bug-killing penicillin could lead to mutant forms of resistant bacteria. Though nobody could argue antibiotics have not reduced human suffering since 1945, their overuse and misuse by the medical profession has created a terrifying list of antibiotic resistant bugs (think MRSA for example) that are killings tens of thousands every year in the U.S. alone and many predict will only get worse…much worse.

The lesson from Fleming and antibiotics – a ‘kill step’ that also has a friendly fire component (as antibiotics also wipe out all the friendly bacteria in your system) – is that panaceas for public health may have unintended consequences. Deadly antibiotic-resistant bugs (though a predicted but unintended consequence) along with the friendly-fire wipe out of good bugs (though not predicted during Fleming’s time but later realized and also unintended, which results in – believe it or not – overgrowth of unfriendly bacteria in the human gut following antibiotic treatment) may have a parallel in our national discussion to zap our fresh produce, which is loaded with millions, and often billions, of benign microorganisms. Their presence is a good thing.

To kill ‘all’ of the bugs on a leaf of spinach, as a casualty of friendly fire during the irradiation kill step aimed at the ‘possible’ contamination from an offending pathogen such as E coli 0157:h7, may have unintended consequences. Mounting research is revealing that humans are too clean and that this is in discordance with our ‘dirty’ past, which literally included being born in the dirt, living in the dirt, eating dirt at every meal, and so on. And we shared this dirty existence with trillions of microorganisms that lived in the same dirt and off the same foods we consumed – thus we consumed them. As a result, humans evolved a symbiotic and organic relationship with these ingested bugs to the point that our immune system has become dependent on them to operate properly.

Our national obsession with hygiene and removing dirt and the bugs from everyday life is giving rise to chronic inflammatory disorders such as allergic disorders (asthma, hay fever), some autoimmune diseases (e.g., type 1 diabetes and multiple sclerosis), and inflammatory bowel diseases (ulcerative colitis and Crohn’s disease). It seems our immune system requires the presence of those dirt bugs to properly function. Without them, the system gets out of balance and overreacts to every little thing.

It was not that long ago that we ate fresh vegetables directly from the garden – minimally processed and no doubt covered in dirt and bugs. Those days are gone. A stroll through your local grocery store reveals neatly wrapped and packaged goodies from industry – all sterile and devoid of dirt and bugs, just what our ‘modern’ lifestyle ordered up. In the 1980s, the leafy green industry started triple washing produce – first a dip into some clean water, followed by a light chlorine bath, then another dip in fresh water. Got to remove those dirt and bugs! But microorganisms that make a living on the surfaces of our iceberg lettuce and spinach – newcomers to the irradiation club – don’t give up their ground easy to a simple triple washing – hence the interest in zapping them (inside and out).

A child born in the U.S. today is likely to live in a sterile future. He has a fifty-fifty chance of being born via caesarean, skipping the trillions of vaginal flora of the birth canal – meaning he will spend the first few hours and days of his life without the benefit of his mothers protective bugs. This, coupled with the likelihood he will consume less breast milk than any previous generation in human history, means he will be endowed with an impaired immune system even before he takes his first step. He will spend his first few months and years of life not crawling around in the dirt and eating bugs as his ancestors did, but playing on indoor carpet and concrete playgrounds all under the watchful eye of parents who will quickly “wet wipe” away any signs of filth – catching the remainder in a nightly bath of suds containing antibiotic substances that will contribute to the antibiotic resistance of a growing menace. He will spend his days downing food-like substances boxed and packaged for maximum cleanliness. And when he moves from the nest and makes his own food choices throughout life, his cart will no doubt be filled with freshly irradiated produce – with no bugs – with a fresh-looking cold pasteurized label.

He will – quite literally – be the sickest generation of our species in human history, though you will not know it. Big Pharma will guarantee he makes it through the day.

Even though the relationship between removing dirt and bugs and the explosion in chronic inflammatory disorders, some autoimmune diseases, and inflammatory bowel diseases is the subject of countless peer-reviewed articles every year, nobody from the CDC, FDA, USDA and so forth has ‘ever’ come to the defense of the harmless bugs on the fresh produce we now seek to zap with irradiation.

Nobody doubts the good intentions of government scientists to improve the health of America, no more than we doubt the meddling of industry and lobbyists to influence those government agencies in directions that maximize influence and ultimately profits. This is how it all works, after all, through the system we support each election year. But lets not suffer from a failure of imagination. A little dirt and a few bugs might be just what the doctor ordered.

A “very” short version of this article appeared in USA Today

While our attention is focused on farm-to-table food safety and disease surveillance once we have gotten sick, the biological question of why we got sick is all but ignored.

Most experts working within what might be called the U.S. Food Safety System, that includes the efforts of some 15,000 people from 15 federal agencies, would readily acknowledge the complexity of detecting the admittedly small numbers of pathogenic bacteria and viruses in the 350 billion pounds of food in a farm-to-table chain that often spans multiple time zones and countries, as an insensitive prevention strategy at best.

Likewise, once an outbreak has been detected, sourcing the offending pathogen can prove difficult, as the ongoing Salmonella Saintpaul outbreak demonstrates even when a genetic match is made. While good farming practices, sampling and testing for detection, and the secondary prevention of tracking down the bad bug once an outbreak has been recognized are critical to a safe food supply, understanding why a person succumbs to what is often a very small number of initial organisms may be a relevant question and an additional strategy in reducing human suffering from foodborne pathogens.

By adding the biological question of why an individuals natural defenses failed to the intellectual concepts of testing, detection, and surveillance, we correctly insert personal responsibility into our national strategy and more importantly, draw attention to the much larger public health crisis, of which illness from foodborne pathogens is only a symptom: our sick, leaky guts.

The CDC warns “The elderly, infants, and those with impaired immune systems are more likely to have a severe illness” associated with tainted food (and water). By “impaired” the CDC is saying that within the complex network of specialized cells and organs that work together to defend against attacks from foreign invaders like Salmonella, something has gone wrong, increasing risk of getting sick – or worse.

A critical component to a properly functioning immune system is a healthy, and balanced population of bacteria. With names like bifidobacterium and lactobacillus, these and other natural inhabitants of the human gut make it their evolutionary job to fight invaders by competing for nutrients (which the invader needs to survive), compete for attachment sites on our intestinal walls (which the invader must do to cause harm), production of organic acids (that the invader does not like), and changing of pH of intestinal ecosystem (which the pathogen does not like either, but fast learning how to adapt). The things that are

This germ-on-germ warfare is literally fought daily in the American gut. When the good guys lose, we know this as diarrhea, fever, and abdominal cramps – or worse. We have all experienced or witnessed these lost battles at varying levels from being restricted to the house, visits to the emergency room, or in some extreme cases, the morgue. While this germ warfare has raged in the human gut as long as humans have been around, the rules of the battle are changing as humanity has started a large-scale experiment by shifting to a highly processed diet that has changed the nutrient supply that our friendly microbes evolved to depend upon.

The irony of the public running from vegetables and fruits that have been suspected in an outbreak, is that these foods contain essential nutrients (dietary fiber) that our gut bugs need to fight the good fight. Our change in diet, coupled with uncontrolled use of antibiotics, may be adversely altering our organic relationship with our most important weapon against foodborne pathogens.

The disruption and increased gut infections caused by pathogens is possibly having an irreversible impact on our entire gastrointestinal system. Like a siege of cannon fire on the walls of a fortress, the walls (barrier) begin to crumble (impaired) and become prone to invasion. Mounting evidence suggests acute and chronic infection by pathogens damage the delicate mucosal barrier that separates trillions of bacteria in our intestinal system from the sterile environment of our blood. As the steady flow of lost battles accumulate, the barrier and our immune system as whole become impaired, resulting in inflammation and movement of pathogens (and endotoxins) into our sterile blood. An impaired and leaky gut barrier plays an important role in a range of maladies such as irritable bowel disease, some cancers, sepsis, organ failure, heart disease and a cascade of other metabolic disorders.

By inserting personal responsibility and some basics of host-pathogen germ warfare into the multi stakeholder strategy for addressing foodborne threats, we may start to realize that we may not simply be experiencing a mathematical rise in foodborne illness as a result of sloppy farming and poor government oversight, but rather a tectonic-like shift in our nutritional landscape that has opened the pathogens door just enough for us to glimpse the future of human suffering. Just the thought makes my gut ache.

Further Reading

Bouhnik, Y., L. Raskine, et al. (2004). “The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study.” Am J Clin Nutr 80(6): 1658-1664.

Cani, PD,  A. M. Neyrinck, F. Fava, C. Knauf, R. G. Burcelin, K. M. Tuohy, G. R. Gibson and N. M. Delzenne  (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia, Volume 50, Number 11 / November

Garcia-Lafuente, A., M. Antolin, et al. (2001). “Modulation of colonic barrier function by the composition of the commensal flora in the rat.” Gut 48(4): 503-507.

Guarner, Francisco (2005). Inulin and oligofructose: impact on intestinal diseases and disorders. British Journal of Nutrition, 93, pp S61-S65

Huerta, M. G. and J. L. Nadler (2002). “Role of inflammatory pathways in the development and cardiovascular complications of type 2 diabetes.” Curr Diab Rep 2: 396 – 402.

Kennedy, R. J., S. J. Kirk, et al. (2002). “Mucosal barrier function and the commensal flora.” Gut 50(3): 441-442.

Kleessen, Brigitta  and Michael Blaut (2005). Modulation of gut mucosal biofilms. British Journal of Nutrition, 93, pp S35-S40
MacFie, J., C. O’Boyle, et al. (1999). “Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity.” Gut 45(2): 223-228.

MacFie, J. (2004). “Current status of bacterial translocation as a cause of surgical sepsis.” Br Med Bull 71(1): 1-11.
Soriani, M., I. Santi, et al. (2006). “Group B Streptococcus Crosses Human Epithelial Cells by a Paracellular Route.” The Journal of Infectious Diseases 193(2): 241-250.

Spiller, R. C., D. Jenkins, et al. (2000). “Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in post-dysenteric irritable bowel syndrome.” Gut 47(6): 804-811.

Zareie, M., K. Johnson-Henry, et al. (2006). “Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress.” Gut 55(11): 1553-1560.

Even though this important reality underlies the basic evolutionary biological principles of modern human nutrient requirements, it is all but missing from policy and research discussions on recommended intake of dietary fibre throughout the world. Even more startling, much of our discussion on the health benefits of fibre, at least in the U.S. and U.K., often refer to the mechanical actions of fibre (stool bulking, for example) and nearly ignores the critical role of dietary fiber as a nutrient base of sorts for the trillions of microbes living throughout the human gut.

It’s safe to say that our current chronic low-intake of dietary fibre in the western world (~12 to 15g/d) – coupled with our overuse of antibiotics and the increase in multiple antibiotic resistance in pathogens – has started a large-scale genetic “re-engineering” experiment on the slowly evolved and critical symbiotic relationship between humans and our little evolutionary hitchhiking friends, with limited discussion of its outcome on public health.

As you read this, there are millions of tiny microbes swimming around in the fluid surrounding your eyeballs. But you can’t see them. There are millions more under your fingernails, on your hands, arms, legs and just about every imaginable section of your fleshy real estate. There are millions more lining your moist nasal passage, many more maneuvering about your liver, heart, lungs, pancreas and trillions more have been living throughout your continuous gastrointestinal tract – from mouth to anus – from the moment you enter this world. But this is good news.

The bad news is as we fill our shopping carts and pantries with the latest neatly boxed and wrapped goodies of industry, we continue down a path that began some ten thousand years ago with the emergence of agriculture – an event that eventually, along with steel roller mills in the 1880s, farm subsidies in the 1970s, and the divergent interests of food sellers and public health, may be leading us on a path to one of the greatest unintended consequences in human history by tinkering with the health of our intestinal microbes. Current dietary advice would be well served by an appreciation that the average human is a complex super-organism, rather than a single individual.

The archaeological and ethnographic record serves as an interesting reminder of the magnitude of the shift in the diversity and quantity of fibre in human diet.

Along the shores of the Sea of Galilee in modern-day Israel, a remarkably well-preserved collection of plant remains recovered from the 23,000-year-old archaeological site of Ohalo II provides an extraordinary window into a broad-spectrum diet that yielded a collection of >90,000 plant remains representing small grass seeds, cereals (emmer wheat, barley), acorns, almonds, raspberries, grapes, wild fig, pistachios, and various other fruits and berries. Owing to excellent preservation, a stunning 142 different species of plants was identified, revealing the rich diversity of fibre sources that was consumed by the site inhabitants.

In Australia, Aborigines are known to have eaten some 300 different species of fruit, 150 varieties of roots and tubers, and a dizzying number of nuts, seeds, and vegetables. Recent analysis of over 800 of these plant foods suggest the fibre intake was estimated between 80 to 130 g/d – possibly more – depending on the contribution of plants to daily energy needs.

In semi-arid west Texas, a nearly continuous 10,000-year record of ancient foraging reveals a plant-based diet that conservatively provided between 100 to 250 g/d of dietary fibre. Analysis of hundreds of preserved human feces (coprolites) recovered throughout the 10,000-year archaeological sequence reveal a significant diversity of plants were consumed.

While the diversity and quantity of fibre varied spatially and temporally in the past, our ancestors clearly evolved on a diet that included daily intake of fibre from a huge diversity of sources that far exceed those recorded among populations in recent intervention and prospective studies concerned with the role of fibre in human health. These modern studies invariably group people with fibre intakes hovering around 20 g/d as the “high fibre” group, when in reality these high fibre or upper quintile groups are in fact low from an evolutionary perspective. Therefore, from an evolutionary perspective we should not be surprised when analytical hair splitting of these minute amounts of fibre does not yield the desired protective role one might suspect going into the study.

The potential protective role of dietary fibre among these modern studies may further be complicated by the lack of diversity as much as the quantity. According to data compiled by the Economic Research Service, United States Department of Agriculture in 2007, 57% of all vegetables consumed by Americans are limited to five sources (potatoes, tomatoes, leafy greens, lettuce, and onions). Unfortunately, the most consumed vegetable in America, the potato, is often in the form of oil-soaked french fries or potato chips. For fruit, five sources (apples, bananas, grapes, strawberries, and oranges) account for 71% of the total intake. From an evolutionary perspective, this minimal diversity, even when coupled with the handful of whole grains and beans/legumes consumed, translates into a striking shortfall in the physical and chemical diversity of fibre once consumed by humans and subsequently utilized by the hundreds of bacterial species that inhabit the human gut. We have changed the rules of the game between “us and them” in such a way as to possibly disrupt the organic harmony that evolved in this symbiotic relationship to a nutritional tipping point.

The emergence of prebiotics as a “super fiber” of sorts is just one example of the importance of diversity of fibre in the human diet. The steady clip of scientific papers demonstrating the health benefits of prebiotics is fascinating as we are literally peaking under the evolutionary curtain of our nutritional past.

Unlike probiotics, which are live microbial organisms that are naturally present in the human body, prebiotics are literally food for probiotics. While many fibres claim to be prebiotics, true prebiotics selectively stimulate the growth of certain probiotics known to be beneficial to humans, such as bifidobacterium and lactobacillus, while not promoting the growth of less useful or even harmful strains, such as clostridium.

Even though prebiotic fibres are present in more than 30,000 edible plants throughout the world, American and European diets only include 1 to 3 g/d – sometimes a little more, sometimes a little less. When we look into the archaeological record, like the west Texas example discussed above, we see daily consumption (though variable seasonally) of 10, 15 and often more than 20 g/d from desert plants such as agave, prickly pear, sotol, wild onions and so forth. Dozens of peer-reviewed studies have shown that test subjects who consumed between 5 to 20 g/d of prebiotic fiber, mainly in the form of inulin and fructo-oligosaccharides derived from chicory roots, were able to stimulate the growth of “good” bacteria and increase calcium absorption, blunt hunger, relieve symptoms of irritable bowel syndrome, reduce biomarkers of some cancers, reduce inflammation through various mechanisms, improve immunity, and fortify our natural defenses against many food-borne pathogens. And the list goes on.

It would be a mistake to look at the science and health benefits emerging from clinical benefits of prebiotics as a new discovery of some magic bullet. More correctly we are simply witnessing a rediscovery of the importance of the diversity of fibre in human diet and, specifically, the role these particular fibres play in the health and well-being of gut bugs.

The exciting science behind prebiotics coupled with the underlying biological reality that humans are still designed to ferment a large and diverse quantity of fibre (~50 to 90 g/d, minimum), and that much of our health is tied to the maintenance of a healthy population of gut bacteria, should serve as a wake up call for new therapeutic approaches to health. We don’t need yet another diet for us, but desperately need a diet for our entire “super-organism’ – both us and them.

Even though humans evolved from nothing more than a run-of-the-mill large mammal on an open savannah of other large mammals, to something of a geological force in an evolutionary blink of an eye, we owe much of our current success as a species to these tiny microorganisms. They require little more than a safe place to live and a steady flow of the quantity and diversity of fibre that they and their microbial ancestors evolved on.

Continuing to ignore our shared nutritional past with our tiny friends and adhering to the very human-like notion that we are somehow separate from nature will only result in progression of many human diseases to levels that will require the medical community to seek new vernacular to describe the public health hardships that potentially lie ahead. Fibre anyone?

So is our food supply less safe and are the growers, shippers and various groups and agencies tasked with oversight not doing all they can to protect the consumer from deadly microbes as some believe? While the media and the public at-large lays blame at the doorstop of industry and government, might the brunt of this burden be misplaced? Simply, are we so involved in finger pointing, fences and hairnets that we don’t see the forest for the trees? An evolutionary perspective on the problem suggests, maybe.

Forgetting for a moment that the latest deadly microbe on the scene originates in cows, one needs to come to grips with the fact that the microbes have us out numbered. When a handful of rich soil contains tens of millions of tiny microbes, and that a single leaf of spinach may be covered in millions more, you start to get a feel for the germ warfare we are up against. Even worse, our so-called modern diet which is dominated by highly-processed grains and added sugars and fats, is putting us at significant disadvantage in the battlefield that is us.

But evolution has equipped humans with an ingenious system for defending against this daily microbial onslaught, most of which are harmless. Our very own microbial foot soldiers, which set up shop in our guts the minute we entered this world. There are so many microbes in the human body that if you added up their total number of cells, they would out number our human cells 9 to 1. In other words, we are more microbe than mammal.

The vast majority of the trillions of bacteria that live in our gut, most of which can be found in our large bowel and represent hundreds of species, make it their evolutionary job to keep out the pathogens that seek to do us harm. In this complex bacterial ecosystem, potentially pathogenic bacteria (e.g., E. coli 0157:H7, Salmonella, Listeria) from the “outside” world are typically suppressed by a mechanism called colonization resistance. Since the human intestinal tract is a continuous system from mouth to anus, anything present within our gut is technically still outside our body. That said, a deadly strain of E. coli does very little harm as it travels through our gut, it’s when it attempts to attach to the wall of our intestinal tract that problems occur.

In order for deadly pathogens to attach, they must compete for nutrients and colonization sites under a steady fire of microbial substances being hurled at them by our resident gut bugs. No doubt about it, this is germ warfare 101 and our gut bugs want to win. If our microbial foot soldiers are successful, then the pathogen cannot gain a foothold and consequently are swept from the system. If they are not suppressed, we quickly become aware of the lost battle from the all-to-familiar gut ache, cramping, and diarrhea, or even worse, death.

This germ warfare has been raging in the human gut for as long as humans have been around. But recently, breath taking changes in our diet has put us at a disadvantage. In order for our gut bugs to fight the good fight, they need nutrients and a critical component of that nutrient base is dietary fiber. By definition, dietary fiber is any part of a plant that cannot be digested and absorbed in the small intestine and ends up in the large bowel (colon). Once in the colon, dietary fiber is broken down and utilized by our good bugs for their own growth. This means, dietary fiber is not food for us but food for the trillions of bacteria that live in our colons. If you feed them, the bacteria will do their evolutionary job and make life a living hell for foreign pathogens.

Our modern genome and the symbiotic relationship we developed with our gut bugs was selected on a nutritional landscape very different from the one we find ourselves today. Our not-so-distant ancestors consumed between 50, 75 and up to often greater than 100 grams a day of dietary fiber. The average American today consumes between 12 to 15 grams. More importantly, our gut bugs evolved on a diet that included an extraordinary variety of fiber sources from hundreds of plants. Humans and our evolutionary hitchhikers went from a large quantity and diversity of fibers, to a small quantity and a limited diversity. We are literally starving our gut bugs to the point that we have opened the pathogen door just enough for E. coli 0157:H7 and its band of pathogenic brothers to compete successfully for nutrients and attachment sites. Not good.

The decrease in quantity and diversity of nutrient sources (dietary fiber) has created a nutritional tipping point in the germ warfare raging in the American gut. While increased oversight, inspections, sampling and stepping up good agricultural practices are important, there are simply too many contamination variables from plough to plate. So rather than look at the recent spike in outbreaks as a result of more pathogens in the food supply and sloppy farming, might the problem have more to do with our own dietary choices. That is, our breathtaking drop in the diversity and quantity of dietary fiber might be the real problem – or at least part of the problem. In other words, dare I say, there is some personal responsibility the American public has in this germ warfare.

When someone spends a lifetime smoking two packs a day, are they not aware that if they succumb to lung cancer, that it’s in affect their own fault? So where is the personal responsibility in our national discussion on food-borne illness and the produce industry we seek to blame? Rather than run from spinach, let us run to it.

As the amount of dietary fiber in the American diet continues to decrease – and probably even more so since last years outbreaks – and our ignorance of the consumers responsibility in this germ warfare continues, we may be seeing a perfect storm of our own creation – though unintended. The litigious atmosphere surrounding this perfect storm has already created the potential for a public that sees diarrhea as a result of a nasty microbe as something akin to a winning lottery ticket. And the situation is likely to get worse.

However, the public’s current mistrust of the produce industry may be an opportunity. Though tragic in its realization, the microscope the industry is currently under may provide a platform to explore some positive steps the industry might take in educating the public about how to increase their natural resistance to food-borne pathogens by returning the quantity and diversity of dietary fiber needed to support a healthy population of gut bugs. By consuming more vegetables and fruits, the American public may be able to add another weapon in our arsenal in our battle with food-borne pathogens and importantly, own some of the responsibility in this germ warfare. Currently, the consumer is totally unaware of the important role they play in keeping themselves and their family members healthy.

The produce industry does not need to wait until tomorrow to start this process, but start today. On September 14, 2006 the produce stepped through a door and there is no going back. It’s time to reposition produce in the American conciseness. The antioxidant and other micronutrient wagons the industry has hitched itself to in the past is tired and the American public has been yawning at that message for years. The American public needs a reason to eat more produce, something new, something fresh. Significant gains may be realized if produce is positioned more as fiber – that is, produce farmers are in fact fiber farmers. This “Fiber Defense Diet” may in fact play a role in a much need rallying call for produce in America and give consumers a very important reason to increase intake.

Some may suggest that the fiber defense argument for fighting food-borne pathogens is too simple, and therefore could not possible make a difference. And they may be right. However, the human immune system and accompanying colonization resistance mechanism that is facilitated by our own natural gut bugs, makes all external attempts such as fences, increased inspections, and triple washing look like child’s play. Our best defense has always been and will always be our natural resistance. Not nurturing our gut bugs with the nutrients they need has consequences. Continuing to ignore this basic tenant of human biology will only result in an increasing number of our fellow citizens in the emergency room and decreased sales at the farm gate.

Sir,

Geoffrey Cannon¹ repeats a widespread affirmation that “paleolithic people usually did not survive into what we call later middle age.” His underlying point, which is widely shared among researchers and the public at-large, is that our ancestors did not live long enough to develop cancer, heart disease and other chronic illnesses. All of which forms the basis for the near universal belief that ancient hunter-gatherers (our ancestors) really were not healthier or fitter than us moderns, and therefore their ancient dietary practices have little relevance to modern health, well-being, and longevity.

On the initial point, Cannon is correct. The average life span of our ancestors was short, compared to that of modern humans in developed countries where one can expect to live into their 60s, 70s and possibly early 80s, on “average.” Conversely, a Neanderthal living in ancient Europe was lucky to live past her teens, and if you lived to your mid-thirties you might have been considered old in Ancient Egypt. More recently, the average life expectancy in the United States in 1900 was 47.3 years. By 1935, that age had risen to 64 years and today that number hovers in the 70s for both women and men (though women can expect to live a few years longer, on average).

The first problem with this thinking is the “average life span” math is misleading and tells us very little about the health and longevity of an individual, but rather gives us an average age of death for a given group or population. For example, a couple that lived to the ages of 76 and 71, but had one child that died at birth and another at age two ([76+ 71 + 0 + 2] / 4), would produce an average life span of 37.25. Using this methodology it is easy to see how one would come to the conclusion that this group was not very healthy.

However, the precept that diet played a significant role in the abbreviated average life span of our ancestors is simply not true. There are few among us that believe are so-called westernized diet of highly processed grains and added sugars and fats are an optimal diet for anyone – past or present. Our soaring rates of obesity and an ever-growing list of acute and chronic diseases – occurring in alarming frequency among younger sections of the population – speak to the discordance.

It is useful to point out that our species reached our current anatomical and physiological standing nearly 200,000 years-ago². That is, while components of what we discern as hallmarks of behaviorally modern, such as language, art, trade networks, and advanced weapons, have only occurred within the last 50,000 years, the hardware has been in place for 150,000 years. While we may drive around in hybrid cars today, we do so in very ancient bodies and with a genome that was selected, for the most part, on a nutritional landscape very different than the one we find ourselves today.

Before the advent and “widespread” adoption of agriculture, which depending on where you lived occurred between 1,000 and 9,000 years ago, humans organized in highly mobile groups of dozens or a few hundred individuals. Archaeological data and analysis of burial populations³reveals that life was harsh and dominated by warfare, strife, destruction, human trophy taking, and the all-to-often practice of infanticide. All of these facts of ancient life, in conjunction with the lack of simple antibiotics and modern surgical practices, resulted in shorter average life spans than many of us enjoy today.

As agriculture took hold around the globe and groups settled down and built more permanent communities and ultimately socio-politically complex civilizations, the more homogenous and centralized food and water supply was easily contaminated by human waste. While war and even larger massacres continued throughout the agricultural revolution, tiny microbial killers took their share of victims, especially among the young and undernourished, further reducing the cyclical nature of the average life span. As European ships set sail just a few centuries ago, new ills and evils further reduced the average life span of populations they encountered – albeit punctuated.

As war, insanitariness, killer microbes, and illness pulsed through humanity over time, our basic underlying physiological and nutritional parameters have changed little in the last few hundred thousand years. Our modern genome is in fact and ancient one and natural and cultural selection has built it to last. Under optimal nutritional conditions, such as those our genome evolved on, us modern hunter-gatherers can live healthy and long lives. We need only look to the modern Hunza of northern Pakistan or the southernmost Japanese state of Okinawa to witness the longevity that our ancient genome is selected for. With the threat of war and violence greatly reduced, and upon a sound footing of a safe food supply, our ancient bodies can be healthy well beyond “our best-before date” Cannon writes about. Based on a low-calorie, high-fiber plant-based diet, a significant portion of the population enjoy healthy and active lives into their 80s, 90s, and often beyond 100⁴. Incredibly, the aged portions of these populations have lower rates of obesity, heart disease, diabetes, hypertension, high cholesterol, cancer, and other chronic diseases compared to western populations.

The modern world owes much to antibiotics and advanced surgical procedures of the last half century, resulting in dramatic increases in average life span for much of the developed and developing world. Though horrific events in Darfur and other African states remind us how significant gains in average life span can easily be erased. In Iraq, a male or female could expect to live to an average age of 66.5 in 1990, but today following years of foreign occupation and endless violence, life expectancy has dropped to a mere 59 for both sexes – and slightly younger for males.

The self-confidence that comforts us today as we review the average life span of our ancestors is misguided and tenuous when viewed through the captivating haze of modern medicine that literally props most of us up into our golden years. I doubt our ancestors would call this living. While we may live longer than our ancestors, we are in fact dying slower. So rather than rest on our perceived cultural and medical success as it pertains to our longevity, we should challenge ourselves and genomes to maximize our health for optimal longevity. For those not trusting of the past and the nutritional landscape upon which we evolved, our genetic cousins, the Hunza and Okinawans, have shown us a way forward.

References

1 Cannon G. Out of the Box. Public Health Nutrition 2007;

2 McDougall I., et al. Stratigraphic Placement and Age of Modern Humans from Kibish, Ethopia. Nature 2005; 433:733-736.

3 Lawrence H. Keeley. War Before Civilization. Oxford University Press, 1996.

4 John Robbins. “Healthy at 100” Random House, 2006.

5 Population Reference Bureau. http://www.prb.org/Countries/Iraq.aspx. Accessed June 9, 2007.

While modern studies continue to expand our knowledge of the health benefits of prebiotics, virtually nothing is known of their use among ancient populations. Drawing on select ethnographic and archaeological data, examples of prebiotic use in ancient diet is presented. By utilizing well-documented cooking facilities found throughout the archaeological record of North America used to cook inulin-bearing plants as a proxy, prebiotic consumption is documented in Europe and the Mediterranean possibly as early as 40,000 years ago. Data is further provided to suggest that early members of the genus Homo had ample ecological opportunity to include prebiotic underground storage organs found throughout the arid African savannah into diet as early as 2.5 million years ago. This cursory view into the nutritional past of our ancestors reveals that prebiotics were likely consumed in quantities higher than seen among modern humans.

Keywords: prebiotics, evolution, archaeology, nutrition, cook-stone technology

Introduction

Since the 1970s, there has been renewed interest between colonic function and human health (Jenkins et al.1999), 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 (Gibson and Roberfroid1995; Gibson et al. 2004; Van Loo 2005). 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 (Roberfroid 2002; Van Loo 2004a, b). Although much current research is aimed at demonstrating health benefits for modern populations, and mechanisms for delivering them safely into the food supply (Franck 2002), very little is known about the consumption of inulin-type fructans throughout human history.

This paper briefly reviews 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 (Leach et al 2006a, b). 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 (Jenike 2001; Jenkins et al.1999). 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 (Cordain et al. 2002; Eaton et al. 2002 ; Goldsmith 1993; Williams and Nesse 1991). 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 (IOM 2002). 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 (Finlayson 2005; Wood 2002). 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 (O’Keefe and Cordain 2004). 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 (Cordain et al 2002; Shephard and Rode 1996) and biomarkers of illness such as rising blood pressure, increasing adiposity, and insulin resistance (Blackburn and Poineas 1983; Glanville and Geerdink 1970; Joffe et al. 1971; Kuroshima et al. 1972; Merimee et al. 1972; Spielmann et al. 1982).

Though traditional hunter-gatherer diet and lifestyle vanished in its ‘purest’ form in the early 20^th century (Murray et al. 2001), 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 (Eaton 2007; Eaton et al. 2002), 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 (Stearns 1999; Trevathan et al. 1999), 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 (Sing et al. 1996). 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 (Milton 1999). 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 (Cordain 2000) 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 (Brand-Miller and Holt 1998; Gould 1980), while Alaskan Artic Eskimos are famous for a diet almost exclusively of raw fat and protein from marine mammals (Ho et al. 1972).

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 (Finlayson 2005; Wood 2002). 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 (IOM 2002; Shuman 1996), 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 in Ancient Diet

The occurrence of the storage carbohydrate fructan in a significant portion (>36,000 species) of the world’s flora (Hendry 1987) 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 (Hatley and Kappelman. 1980;Laden and Wrangham 2005). Today, many of these same resources serve as staples for the modern foragers and farming groups still inhabiting the same subtropical environs (Murray et al. 2001; Vincent 1985). 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 (Ragir 2000; Stahl 1984). 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 (Van Loo 1995).

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 (Lee-Thorp et al. 1994; Richards et al. 2001). 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 (Wandsnider 1997), 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 (Sobolik 1990).

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 (Bousman et al. 2002). 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 (Thies 1990). 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 (Leach 2005). 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 (Thoms 2003).

The reoccurring use of large, rock-lined earth ovens, which are often associated with cooking of inulin-rich plants (Wandsnider 1997), is well-documented in the historical and ethnographic records for North America and northern Mexico. For example, Castetter et al. (Castetter et al. 1938) 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 (Leach et al. 2005). Synthesis of hundreds of radiocarbon dates from cook-stone facilities across extensive areas of southern North America (Leach 2005) 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 (Leach 2005; Wandsnider 1997).

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 (Holdaway et al. 2002). 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 (Brock 1988).

Among the 800 plus plant foods known to have been eaten for tens of thousands of years by Aborigines in Australia (Brand-Miller and Holt1998), many were tuberous roots and corms that contained prebiotic inulin (Van Loo 1995) and required prolonged cooking in rock-lined pits (Gott 1982; Gould 1980; Incoll et al. 1989).

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 (Movius 1963). 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 (Thoms 2003), 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 (Dogome 2000). 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 (Dogome 2000). 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 (Leach 2005).

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 (Pazola and Cieslak 1979; Van Loo 1995). 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

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. (Van Loo 2004a, b, 2005).

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 (Mellars 1996), 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 (Steiner 2002), 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 (Holly 2005; Thoms 2003) 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 (Schlicting and Pigliucci 1998). 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 (Schell et al. 2002) 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 (Leach 2007). 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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Table 1. A sample of inulin-containing plants identified as food among

indigenous populations (adapted from Wandsnider 1997).

* Over 300 species of agave have been reported throughout the American Southwest and northern Mexico (Gentry 1982), all of which are thought to contain inulin.

Unfortunately, this well-intended legislation will fall short of anything meaningful, as its patrons most certainly fail to understand the basic evolutionary rules of the germ warfare raging in the American gut and the bigger challenges facing the populace in this biological arms race.

As executives of the produce industry hit hardest by the illness and deaths attributed to E. coli 0157:H7 in 2006 brace for a possible onslaught of new regulations and additional inspectors trudging about their fields and packaging plants, they need only look out to the fields beyond their office windows to see a better solution to what ails them and the American public.

Among the lush greens, yellows and reds of the American produce landscape, lies a simple, but critical component, to our evolutionary success as a species and the best defense we have ever had – or will likely ever have – against reducing our risk from E. coli 0157:H7and the assortment of pathogens that seek to do us harm on the biological battle field that is us.

The simple defense to be found amid these fields is good old dietary fiber.

As you read this, there are trillions of tiny microbes (including billions of harmless strains of E. coli) living throughout your continuous gastrointestinal tract – from mouth to anus. These tiny evolutionary hitchhikers have been with you every minute of every day from the moment you entered this world and will be so until you die. And then they will eat you. But that’s the good news.

The bad news is our so-called modern diet of highly processed fiber poor grains, in addition to added sugars and fats, is literally starving our “friendly” bacteria and putting us at increased risk. The friendly bacteria in our bodies are the first line of defense against invading pathogens, such as E. coli 0157:H7. Like any good soldier they require nutrients to fight the good fight and dietary fiber is an important part of that nutrient base.

Simply stated: Fiber is not food for us, it’s food for bacteria that live in our gut.

Our not-so-distant ancestors regularly consumed between and often more than 50 and 100 grams of dietary fiber from diverse sources every day. This is the nutritional reality upon which our modern genome was selected and the symbiotic relationship which the trillions of bacteria in our gut evolved to depend upon.

However, the average American today consumes about 12 to 15 grams a day – roughly half of what the government recommends and only a fraction of what our gut bugs need in order to resist infection and disease caused by a steady stream of pathogenic bacteria and viruses that enter our gut every day.

No amount of government oversight will ever completely remove the threat of pathogens in our food supply. There are too many variables from plough to plate – not to mention that the bad bugs have us out numbered.

While a cleaner and safer food supply has allowed our species to maintain mammalian dominance, we must not lose sight of the delicate nutritional requirements of our friendly gut bugs and the indispensable role they play in our tenuous existence on this microbe-dominated planet.

The health implications of our staggering drop in consumption of dietary fiber has opened the door to E. coli 0157:H7 and its band of pathogenic brothers who make millions of people sick every year, sending hundreds of thousands to the emergency room with diarrhea, bloody diarrhea, intestinal cramping, and fever, and sending an increasing number of us, to the morgue.

The important symbiotic relationship we share with our friendly microbes and their role in our natural resistance to infection should be taking center stage in the upcoming Congressional hearings on how to best protect “the people” from the inevitable food-borne pathogens associated with produce, and specifically, how to deal with this monster E. coli 0157:H7.

The recent outbreaks have understandably made the American public skittish not only about spinach and other produce tainted with E. coli 0157:H7, but about produce in general. This may pave the way for an additional decrease of fiber in the American diet, resulting in poorer gut health and reduced ability to resist infectious agents.

The media attention given to E. coli 0157:H7 in 2006 has once again raised the awareness of deadly pathogens in our environment. This may be an opportunity, though tragic in its realization, for industry and the government to highlight the importance of increasing fiber intake via fruits and vegetables. Current government health messages to do so have had little success. Maybe it’s time to change the message.

For E. coli 0157:H7 specifically, stimulating the growth of a group of healthy bacteria in the human gut known as bifidobacterium by consuming special prebiotic dietary fibers known as oligosaccharides – found in plants such as onions, leeks, garlic, chicory, and artichokes – can fortify our natural resistance.

Bifidobacteria exert powerful effects against pathogens through competition for colonization sites and nutrients in the gut, acid excretion and antimicrobial peptides. If properly fed and stimulated, these bacteria will do their evolutionary job and make life a living hell for invading pathogens.

Interestingly, bifidobacterium dominate the gut of breast fed babies, but are known to decrease significantly as people get older. This may explain that even though a number of age groups were sickened during the 2006 outbreaks, two out of three of the deaths were elderly women. The third was a 2 year old boy. A similar pattern was seen in a deadly outbreak in Scotland in 1986 that affected hundreds and killed 20. All deaths were among the elderly.

At a time when researchers are finally acknowledging that nearly 20% of all cancers are caused by infection – up from zero just a few decades ago – and with hints that infection may play a causal role in such big time killers as breast cancer and atherosclerosis, it may be time to start asking who or what opened the pathogens door.

Ignorance of evolutionary biology and the nutritional landscape upon which humans and our microbes evolved should not preclude lawmakers and industry from exploring the role of dietary fiber in reducing our casualties in this evolutionary arms race. Continuing to ignore this simple and easy-to-implement strategy will only result in further human suffering.

I, for one, will be having a salad tonight.

*Comments about this article would be most welcome (E-mail).

Further Reading

Mixed culture fermentation studies on the effects of synbiotics on the human intestinal pathogens Campylobacter jejuni and Escherichia coli.
Anaerobe. 2003 Oct;9(5):231-42.

Pathogen survival in the external environment and the evolution of virulence. Biol Rev Camb Philos Soc. 2004 Nov;79(4):849-69. Review.

Evolutionary perspective on dietary intake of fibre and colorectal cancer. Eur J Clin Nutr. 2007 Jan;61(1):140-2.

Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc Natl Acad Sci U S A. 2006 Jun 20;103(25):9667-72.

Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium. J Appl Microbiol. 2006 Apr;100(4):846-53.

Cochran, Gregory M. “Infectious Causation of Disease: An Evolutionary Perspective” Perspectives in Biology and Medicine – Volume 43, Number 3, Spring 2000, pp. 406-448

Evolutionary health promotion. Prev Med. 2002 Feb;34(2):109-18. Review.

Human Evolution, Nutritional Ecology and Prebiotics in Ancient Diet. Bioscience & Microflora Vol. 25, No. 1. pp 1-8

“Children on the frontline against E. coli”: typical hemolytic-uremic syndrome. Clin Lab Sci. 2005 Spring;18(2):90-9.

Prevalence and risk factors of genital Chlamydia trachomatis infection. Medicina (Kaunas). 2006;42(11):885-94. Review.

Introducing inulin-type fructans. Br J Nutr. 2005 Apr;93 Suppl 1:S13-25. Review.

Non-toxic potentiation of cancer radiotherapy by dietary oligofructose or inulin. Anticancer Res. 2002 Nov-Dec;22(6A):3319-23.

Inulin/oligofructose and anticancer therapy. Br J Nutr. 2002 May;87 Suppl 2:S283-6. Review.

The association of Helicobacter pylori infection with the development of gastroesophageal reflux disease (GERD). J Egypt Public Health Assoc. 2001;76(3-4):265-79.

As you read this, there are millions of tiny microbes swimming around in the fluid surrounding your eyeballs. But you can’t see them. There are millions more under your finger nails, on your hands, arms, legs and just about every imaginable section of your fleshy real estate. There are millions more lining your moist nasal passage, many more maneuvering about your liver, heart, lungs, pancreas and trillions more living throughout your continuous gastrointestinal tract – from mouth to anus. And as you ponder this unimaginable invasion of invisible aliens, there are millions more setting up new beach heads on that all-important organ between your ears every minute of every day from the moment you entered this world. But that’s the good news.

The bad news is we are literally starving, depressing and killing off an alarming number of these little evolutionary hitchhiking friends with our so-called modern, westernized diet. Our modern food supply, with its 300,000 or so processed products for sale in the U.S alone, is one stunning example of the cultural, technological and political prowess of a species gone wild. So freakish is our modern food supply, I doubt our ancestors would recognize much of it as food at all. Our internal ‘friendly’ bacteria are equally puzzled.

As we fill our shopping carts and pantries with the latest neatly boxed and wrapped goodies of industry, we continue down a path that began some ten thousand years ago with the emergence of agriculture – an event that would eventually, along with steel roller mills in the 1880s and farm subsidies in the 1970s, lead to the greatest “unintended consequence” in human history: The shift in how and where the human body captures much-needed energy (calories) to power our demanding bodies and lifestyle. Let me explain.

This admittedly dramatic pronouncement – “the greatest unintended consequence in human history” – underlies something I have come to call the Human Hybrid. The Human Hybrid is an evolutionary-based way of thinking about nutrition and the tragic epidemic of obesity and its growing list of acute and chronic byproducts (disease). But nowhere is the Human Hybrid more potentially applicable than when trying to wrap your head around the metabolic syndrome of insulin-resistance (sometimes referred to as Syndrome X). If you are overweight, diabetic, have hypertension, low HDL-cholesterol levels, high triglycerides, or have ever suffered a mild heart attack or stroke, then you probably have the insulin-resistance syndrome. More on this in a moment.

The easiest way to begin to explain the Human Hybrid is to think about hybrid cars – the latest must-have techno gadget for the social and environmentally conscious – and financially stable – among us. The concept behind hybrid cars is simple: a mixture of power technologies such as internal combustion engines and electric batteries (and in some cases electric motors) are applied to create a more efficient system. In other words, two power sources. On the front end you have a gas-powered engine that works to push the car forward part of the time, with the second power source (batteries) in the backend making up the difference a certain percentage of the time.

The clever engineers who devised the hybrid car designed it to run on both sources – not one or the other full-time. They share the work. Running the entire system on one or the other exclusively, would result in the system malfunctioning and falling part. The two energy system was designed to share in delivering the power needs. Like the hybrid car, humans have two major power sources – one in front end (small intestine) and the other, quite literally, on the back end (the colon).

Our Human Hybrid is a hold over from our days of hanging out with other primates and enjoying those low-energy dense meals of roots, leaves, fruits, bark, seeds, insects, and flowers. The good ol’ days. Between 5 to 7 million years ago, the diet of our ancestors – who looked nothing like us at the time, and pretty much like our friends at the zoo – was dominated by lots and lots and lots of fiber. To extract enough calories from this bulky diet, our early tree swinging cousins relied on millions of years of co-evolution with an unlikely cast of microscopic hitchhikers and some ingenious arrangements.

As food passed through our early ancestors stomach and small intestine, enzymes broke down the material allowing for fats, proteins, carbohydrates, minerals, vitamins and so on to be absorbed. Anything not broken down (fiber) was moved on. By definition, fiber is pretty much anything that escapes digestion and absorption in the small intestine and ends up in the colon – end of the line. Far from being wasted plant material at this last station in the gastrointestinal system, the trillions of bacteria that lived in our early ancestors colons went about the task of breaking down that fiber through a process called fermentation and turning it into energy. The bacteria relied on this “fiber” to live (i.e., fiber is food for bacteria!). In the process of fermentation, a byproduct known as short chain fatty acids, with names such as acetate, butyrate and propionate, were generated and then absorbed and used by cell and organs of the body as energy. Voilà! Energy (calories) from bark.

Rough estimates suggest that our early ancestors generated as much 25 to 35% of their energy needs by this hybrid energy technology. Primates living today still rely on the bacteria and the energy they generate to continue to make a living on the lush greens of the world’s tropical – but shrinking – forests.

As our earliest ancestors took those first tentative steps onto the open savannahs of Africa – and began their march to global mammalian dominance all those millions of years ago – they took with them this fully-developed hybrid energy technology and its bacterial power plant for the evolutionary ride. Today, this same cast of characters is still with us, known by names like bifidobacterium and lactobacillus (If you eat yogurt you will recognize these names as they are added today under the heading of probiotics).

But during that long march that ultimately ended in us, our diet improved as we explored new lands and developed technologies to extract more energy and nutrients from our environment. Over each new horizon, novel plants and animals presented themselves – and we ate them. We learned to fish, hunt, and to master fire – cooking food, making it more digestible and unlocked nutrients in quantities and diversities never before seen in primate-human history. And then within the last 10,000 years or so, pay dirt – agriculture, pottery, towns, cities, the wheelbarrow, Roman bathhouses! We never looked back.

As the quality and diversity of diet improved with every novel plant and animal we added to the menu, we digested and absorbed more and more energy and nutrients in our small intestine – the front power plant in our Human Hybrid. Through time, this resulted in an increase in the size of our small intestine to handle the windfall. Over the course of a few million years, our small intestine essentially doubled in volume – thus increasing the amount of energy absorbed in the front end. On the flipside, our colon (back end energy source), with its reduced role as a function of us eating less and less fibrous material, reduced in size by more than half (Click here for a colorful graph comparing the stomach, small intestine, and colon of modern humans to that of modern primates).

Nevertheless, our modern colon still accounts for approximately 20% of the total volume of our omnivorous gastrointestinal system. Compared to the colon of meat-eating carnivores, such as the wolf, it’s down right huge.

The simple fact that the colon still represents a significant portion (by volume) of our modern gastrointestinal system, speaks to its continued and important role in our Human Hybrid as an energy source. If we did not need it to generate energy, evolution would reduce its size, say to that of a strict carnivore. Put another way: though our genome has evolved to less dependence on fibrous plant material through time, the fermentation factory – and its bacterial workers – is open for business today and will likely be so into the foreseeable future (a few hundred thousand years without a doubt).

So 1,300 words or so later, you are probably wondering what this has to do with obesity and diabetes among the Pima Indians of Arizona or for modern humans in general. Quite alot, actually.

Even though our modern colons still occupy an important place in our gastrointestinal system and our overall nutrition, and the lights are on in the fermentation factory and trillions of bacteria (some 1,000 plus species) are standing at their stations waiting to do what they do best, our so-called modern and technically slick food supply and industrial and political landscape over which it flows, have something else in mind – and fiber (food for bacteria and fuel for the backend power station of the Human Hybrid) ain’t it.

By all estimates, modern humans should still be generating between 12 to 18% of our daily basal energy needs from the colon part of the Human Hybrid system through fermentation of dietary fiber. For the average American or European who consumes a scant 12 to 15 grams of dietary fiber a day, the energy being provided by the backend is somewhere less than 5% – even less for some. So how does this short fall translate into something tangible for or about modern human health? Quite simply, it means the front end component (small intestine) of the Human Hybrid is providing the majority of the energy demands and in the process, being over worked – exactly what we do not want in a hybrid system of any kind.

The overworking of the front end is coming in the form of rapidly digested and absorbed foods that dominate our modern diet. This includes all those foods our ancestors would not recognize that are laced with added sugars, fats and highly processed nutrient- and fiber-poor grains (think sodas, ice cream, donuts, most breads, chips, most pizzas and burgers, a lot of the dairy products, and so on). As we eat more and more of these front end fuels, we are eating less of the backend fuel (fiber). The average American and European is getting nearly 60% to 70% of their total daily calorie needs from these front end fuels. This would be like pouring kool-aid in your gas tank and expecting everything to run the same as usual. Something has to give, and it is. Enter the hormone insulin and insulin-resistant syndrome – a root problem in a staggering number of modern ailments.

Since this important story needed to be told in such detail – hence it’s length so far – I will restrict the remainder of the discussion to the development of diabetes and the role of the Human Hybrid (hang in there almost done!).

The eating habits of our ancestors more or less adhered to the Human Hybrid diet that developed from the nutritional landscape on which our genome was selected. Our food supply consistently included up to and more than 100 grams of fiber a day – sometimes more, sometimes less. This meant our “minimally processed foods” contained copious amounts of slowly digested carbohydrates – an essential fuel for the red blood cells and brain, and the main source of energy for muscles under conditions of exercise (something that characterized everyday life for our ancestors).

For over 99% of human history (>2 million years), our ancestors main source of carbohydrates (primary energy source) were wild plants foraged from the ancient landscape. The sugars and starches (carbohydrates) in these plants were broken down by the enzymes in the mouth, stomach and small intestine (front end of the Human Hybrid) and absorbed into the blood stream along with other nutrients and utilized by the cells as energy.

Plant parts that are, due to their either chemical or physical structure (fiber), not broken down in this front end of our Human Hybrid are moved along to the next energy station, the colon.

The most common and important of these energy sources is glucose – a building block of starch. Once glucose is absorbed into the blood stream the pancreas jumps into action and excretes the hormone insulin that binds with the glucose and allows it to be utilized as energy. A cellular key of sorts. Without insulin, the glucose cannot be utilized. And this is where the problem begins.

Our ancestral diet of was ideal because it provided slowly-released energy in the form of slowly absorbed foods (today we know this as a low glycemic diet). This also helped to delay hunger pangs well after a meal and importantly, it was easy on the insulin secreting cells of the pancreas and did not overwhelm the system with too much insulin or glucose. This system of gradual absorption of glucose and excretion of life-giving insulin was what our ancestors evolved on for millions of years and what our genome was selected upon. Like the very specific engineering of a hybrid car – which requires finely tuned inputs and interactions between components with everything operating just as engineered or else things don’t function properly – our Human Hybrid was built in a similar Wikipedia-like way with slow and gradual shifts in diet over huge spans of time – evolutionary time.

Our recent adoption (mainly in the last 200 years, but more so in the last 30) and obsession with industry and government promoted “quick” energy in the form of easily digested and absorbed sugars and highly-processed grains, is throwing everything off. (To get my take – rant – on the U.S. Food Pyramid click here).

When we start overwhelming the finely tuned Human Hybrid with too much glucose from highly-processed foods we are asking the pancreas to excrete more and more insulin at a faster rate. At the same time, we are also bombarding the cells in our muscles and organs with this never-ending flood of glucose and insulin at a rate and quantity never before seen in human history – something they were not engineered to handle. Asking the insulin-generating pancreas to put in overtime often (and usually does) results in it finally malfunctioning (lower insulin levels) or giving out entirely. Without insulin to bind with, the glucose stays in the bloodstream. We know this condition of too much blood glucose as hyperglycemia, or by its more common name, diabetes (type 1 diabetes, of course, is when the pancreas can no longer produce insulin).

Of specific interest to our Human Hybrid is insulin-resistance, which occurs when the normal amount of insulin secreted by the pancreas is not able to unlock the door to cells.  To maintain normal blood glucose, the pancreas secretes additional insulin.  In some cases, when the body cells “resist” or do not respond to even higher levels of insulin, glucose builds up in the blood resulting in the dreaded type 2 diabetes.

So why do the cells resist this much-needed energy? Like a sponge full of water, the cells are saying “enough!” – even when they are not full. Have they become exhausted from trying to keep up with all that insulin and glucose? The science says, maybe – most likely, yes. We know that our unfamiliar, rapidly absorbed, diet is triggering some deeply buried genetic instruction to do so. In other words, the Human Hybrid is out of whack.

And for the Pima Indians of southern Arizona, with the highest recorded rate of diabetes of any group on the planet, it seems to be “just a little” bigger problem. What in their evolutionary past – or more correctly, their nutritional past – predisposes them to this terrible disease over, say, a European? I think it might be in the “fine-tuning” or “final touches” on their Human Hybrid fuel system.

Up until about 10,000 years ago, all humans on earth were hunter-gatherers – making a living on wild plants and animals gathered about the landscape. No pottery, no agriculture, no animal husbandry. Pottery and agriculture first took hold in southeastern Asia, then Mediterranean and then spread throughout what is today modern Europe. So over a period from 5,000 to 10,000 years ago just about everyone in Europe was making a living on a limited number of agriculture products and cooking pots (minus a few pockets here and there). For our Human Hybrid, this meant easier to digest grains – shifting from whole grains to minimally processed ones. And as the grains become smaller and smaller (think coarse flour) with each new grinding technology, the sugars and starches become more digestible and thus required “slightly” more insulin for these increasing levels of glucose in the bloodstream. So far so good, as the process was slow and gradual taking place over thousands of years.

But for the Pima of southern Arizona, dependence on finer and finer flours from cultivated grains occurred much later. Throughout much of the American Southwest people started dabbling with agriculture about 3,000 to 4,000 years ago – but it was not until about 1,250 years ago that it started to dominate the menu. This is thousands of years after it already took hold in the ancient European diet. And for the arid American Southwest, the recent agricultural grain diet was heavily subsidized by a broad spectrum menu that still included an extraordinary variety of wild plants – hundreds of species.

So while Europeans were starting to introduce more rapidly absorbed agricultural grains and seeking acceptance from the genome through making slight dietary adjustments (slow ones) to the Human Hybrid engineering (i.e., shifting more of the energy demands to front end – less fiber that is), our Pima friends were still clicking along on the same diet and Human Hybrid blueprint. They would not start to challenge their genome for thousands of more years.

On top of this, the Pima were late comers to the pottery barn – only developing these handy cooking and storage vessels in any appreciable quantities about 1,800 years ago – thousands of years after there European counterparts. Pottery was a significant engineering change to the Human Hybrid as cooking as heat and water make plant foods more digestible. During cooking, water and heat expand the starch granules, making it easier for the enzymes to break them down, and thus to absorb.

So when you fast forward to today and level the playing field with our modern diet – everyone has equal access to the same technology and foods – the Pima may suffer just a little more because engineering changes to the Human Hybrid in the form of novel foods (agricultural grains) and technologies (cooking pots), genetic requests if you will, were introduced later in their evolutionary history. Thus, their genome has had less time to “try” (and I stress try) to adapt. On a metabolic level, this means when you a challenge a Pima Indian Human Hybrid system with more and more rapidly absorbed foods, their tissues exert a hyper reaction and become insulin-resistant just a tad quicker. This basic premise is similar to the issue of lactose intolerance – with some people who have been exposed to the lactose in the milk of domesticated animals for longer periods of time – suffering less from its affects.

And on one final note about the Pima Indians, their ancestors inhabited the arid lands of the American southwest for thousands of years, where the available edible biomass – both plants and animals – is dominated by fiber-rich plants. In other words, arid environments are dominated by plants not animals and the plants are, as a function of their survival mechanisms in such settings, heavy on the fiber side of things – both soluble and insoluble fibers. In fact, when the ancestors of the Pima got around to growing corn, squash and beans (big time) about 1,250 years ago, they also planted fields and fields of the desert succulent agave (agave is the same genus that is used today to make that delicious tequila!).

So if you squint just a little bit as you look back in time at the Pima ancestors, you see not the famous maize farmers of the American Southwest, but rather you see fiber farmers maintaining their Human Hybrid just as their ancestors had done before them and there descendants will need to do today if they want to break the cycle of disease and misery that a modern/processed diet has brought to these people.

How’s your Human Hybrid?