Beyond Ötzi: European Evolutionary History and its Relevance to Diet. Part III

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In previous posts, I reviewed some of the evidence suggesting that human evolution has accelerated rapidly since the development of agriculture (and to some degree, before it).  Europeans (and other lineages with a long history of agriculture)  carry known genetic adaptations to the Neolithic diet, and there are probably many adaptations that have not yet been identified.  In my final post in this series, I'll argue that although we've adapted, the adaptation is probably not complete, and we're left in a sort of genetic limbo between the Paleolithic and Neolithic state. 

Recent Genetic Adaptations are Often Crude

It may at first seem strange, but many genes responsible for common genetic disorders show evidence of positive selection.  In other words, the genes that cause these disorders were favored by evolution at some point because they presumably provided a survival advantage.  For example, the sickle cell anemia gene protects against malaria, but if you inherit two copies of it, you end up with a serious and life-threatening disorder (1).  The cystic fibrosis gene may have been selected to protect against one or more infectious diseases, but again if you get two copies of it, quality of life and lifespan are greatly curtailed (2, 3).  Familial Mediterranean fever is a very common disorder in Mediterranean populations, involving painful inflammatory attacks of the digestive tract, and sometimes a deadly condition called amyloidosis.  It shows evidence of positive selection and probably protected against intestinal disease due to the heightened inflammatory state it confers to the digestive tract (4, 5).  Celiac disease, a severe autoimmune reaction to gluten found in some grains, may be a by-product of selection for protection against bacterial infection (6).  Phenylketonuria also shows evidence of positive selection (7), and the list goes on.  It's clear that a lot of our recent evolution was in response to new disease pressures, likely from increased population density, sendentism, and contact with domestic animals.

Why are modern human populations riddled with these common deleterious mutations?  Presumably, these are "genetic shrapnel" that result from rapid changes in the human environment, creating selective pressures that placed strong new demands on the genome.  The modern form of malaria is only a few thousand years old, corresponding roughly to the development of agriculture in Africa and the high population densities that resulted (8).  As soon as malaria evolved into its modern deadly form, there was a massive selective pressure to evolve resistance.  Resistance would be favored at almost any cost, even if it meant that a percentage of offspring would wind up with a serious disorder and probably not reproduce.  So humans evolved this crude stopgap measure, which basically deforms the hemoglobin molecule and makes red blood cells more difficult to infect by malaria parasites.  It also deforms red blood cells into a "sickle" shape if you get two copies, resulting in disease symptoms.

Even the less deleterious mutations like lactase persistence (allows digestion of the milk sugar lactose) are crude.  The mutation that causes lactase persistence basically breaks the genetic "switch" that turns off lactase production after infancy.  In genetics as in life, it's much easier to break something than to build it, so these kinds of mutations are the low-hanging fruit.

Presumably, with time, natural selection would figure out a better way of doing the same thing-- a more sophisticated genetic measure that could fill in for the crude stopgap, which would then fade away.  This is the key principle I'm trying to illustrate with these examples: the crudeness of recent adaptations suggests that we're still in the early phase of genetic adaptation to the Neolithic environment.  Much of the low-hanging fruit has been picked, but I suspect there's a lot of fruit higher up that would also get picked if we had another million years to evolve (assuming our environment remained stable, which it won't).  In other words, I suspect most of us reading this are partially, but not completely, adapted to the Neolithic diet.

Evidence that Adaptation to the Neolithic Diet is Incomplete

Previously, I cited celiac disease as an example of incomplete adaptation.  Affecting just under one percent of US citizens, it's a serious autoimmune disorder that's provoked by gluten from wheat and other gluten grains.  This is a major public health burden coming from a single food type.  On further reflection, I think this isn't a good example of incomplete adaptation, because the gene that confers gluten sensitivity was under recent positive selection.  In other words, the people who first domesticated wheat probably weren't genetically susceptible to celiac disease, but they later acquired it through a twist of genetic irony (9).  Some geneticists suspect the gene confers disease resistance that outweighs its detrimental effects.  Live and learn.  Thanks to Melissa McEwen for pointing this out to me.  I think she heard about it from John Hawks.

Still, I'm drawn to the evidence that early agriculturalists showed signs of nutritional stress.  From Health and the Rise of Civilization, by the anthropologist Dr. Mark Nathan Cohen:

A second common trend is that farmers appear to have been less well-nourished than the hunter-gatherers that preceded them, rarely the reverse.  For example, rates of porotic hyperostosis (suggestive of anemia) are almost universally higher among farmers in a region than in earlier hunter-gatherers in the same region. [he goes on to suggest that this can result from increased parasite load in addition to an iron-poor diet- SG].

Other independent measures of nutrition are less widely reported but most often seem to suggest a decline in the quality of nutrition associated with the adoption and intensification of agriculture.

In the same book, Dr. Cohen comments on the better nutritional state of modern-day hunter-gatherers relative to non-industrial agriculturalists with poor access to animal foods and low diet diversity:

...levels of meat intake reported for most hunter-gatherer groups are comparable to intake by relatively affluent modern Western populations.  They are substantially better than average Third World intake and dramatically better than that of the contemporary third world poor, who may average only a few grams of animal foods per person per day.

A wide range of reports about contemporary hunter-gatherers in various parts of the world suggests that they, like the San, eat eclectic diets of fresh vegetable foods that, along with their meat intake, tend to assure a good balance of vitamins and minerals.  These observations about dietary balance are largely confirmed by reports and observations on hunter-gatherer nutritional health.

Most casual descriptions of hunter-gatherer groups in tropical or temperate latitudes comment on their apparent vitality and the absence of obvious malnutrition...  Reports of acute malnutrition or kwashiorkor are extremely rare [kwashiorkor = protein deficiency- SG].  These descriptions present a striking contrast to descriptions and evaluations of many Third World populations and to descriptions of historic dietary quality for the lower classes in Europe.

It's a great book if you haven't read it.  Anyway, the main point is that hunter-gatherers, living the deep ancestral lifestyle, are generally better nourished than agriculturalists with diets restricted mostly to grains and with poor access to animal foods, and this was particularly true of early adopters of agriculture.  However, the nutritional status of agriculturalists improved over time, presumably because of the introduction of complementary foods (domestic animals, legumes, vegetables, etc.), preparation methods (e.g., fermentation), and genetic adaptations.

If we look for it, there is plenty of evidence to be found that a grain-heavy diet is not optimal, especially in the context of low animal foods.  Children are particularly sensitive, while adults are fairly resistant to the negative effects of extreme diets.  For example, the macrobiotic diet is based around whole grains, legumes, vegetables, and some fruit, and typically contains no animal foods.  It's not a third world diet-- it's a diverse, whole food-based diet that's composed with great care.  It doesn't take much digging to find evidence of deficiency diseases in macrobiotic children, including rickets (10), vitamin B12 deficiency (11), and assorted mineral deficiencies.  Here's a quote from a survey of macrobiotic children conducted in the Netherlands (12):

Ubiquitous deficiencies of energy, protein, vitamin B-12, vitamin D, calcium, and riboflavin were detected in macrobiotic infants, leading to retarded growth, fat and muscle wasting, and slower psychomotor development. Breast milk from macrobiotic mothers contained less vitamin B-12, calcium, and magnesium.

There are a number of nutritional problems with grains, particularly whole grains, that emerge when they make up too large a proportion of the diet.  One of the key problems is that although whole grains contain a sufficient quantity of many minerals, the availability of these minerals is often low because they're bound by phytic acid.  Much of it just ends up in the toilet.  This is why mothers on a macrobiotic diet, eating large amounts of magnesium-rich brown rice, end up with magnesium-deficient milk.

This explains why cultures that rely too heavily on whole grains (particularly unfermented) can end up with mineral deficiency symptoms despite a seemingly adequate supply of minerals in the diet.  One example is rickets.  Normally associated with vitamin D deficiency, it can also be caused by mineral deficiency, principally calcium, even when vitamin D status is good.  In Dublin in 1942, the incidence of rickets rose sharply, coinciding with a switch from refined wheat flour to whole wheat flour.  Investigators had this to say about it (13):

It therefore appears likely, as Jessop (1950) suggested, that the major change in the
extraction rate of the flour used as a staple item of diet in Ireland was responsible for a marked simultaneous rise in the incidence of rickets, independent of changes in vitamin D intake [or sun exposure- SG]. This hypothesis is supported by the subsequent decline in the incidence of rickets in older children between 1 and 4 years as the extraction rate of flour was reduced. The observation that the incidence of rickets changed little in children under 1 year who consumed little or no bread is consistent with this hypothesis...

The traditional Asian [they mean Indian here- SG] diet contains much unleavened high-extraction cereal as chapatty and a variety of pulses. In Iran Amirhakimi (1973) and Rheinhold (1971) found rural rickets in children whose sunshine exposure appeared normal but whose diets contained large quantities of unleavened wholemeal bread as tanok. In rural Kashmir Wilson (1931) found severe osteomalacia in field workers who spent many hours a day outdoors but whose diets were exclusively vegetarian, consisting almost entirely of rice, lentils (dal) and wholewheat flour (atta). Pettifor et al. (1978) found severe adolescent rickets in rural Bantu children in Natal whose diet consisted almost exclusively of maize and green vegetables; their sunshine exposure was high.

Investigators have shown that a diet high in unleavened whole grain bread causes mineral loss from the body over time, and this cannot be corrected by supplementing vitamin D (14, 15).  These diets lead to zinc deficiency as well, and correcting this deficiency alleviated growth stunting in Iranian children eating a diet rich in unleavened wheat bread (16).

Heavily grain-dependent cultures also often show signs of severe vitamin A and protein deficiencies (17).  Dr Edward Mellanby commented on the high susceptibility to infectious disease in the agricultural Kikuyu tribe compared with their neighbors the milk-drinking Masai, who also physically dominated the Kikuyu and other surrounding agricultural groups.  Based on his studies of vitamin A and infectious disease resistance, he attributed this in part to better vitamin A status among the Masai (Edward and May Mellanby. Nutrition and Disease. 1934):

The high incidence of bronchitis, pneumonia, tropical ulcers and phthisis among the Kikuyu tribe who live on a diet mainly of cereals as compared with the low incidence of these diseases among their neigh­bours the Masai who live on meat, milk and raw blood (Orr and Gilks"), probably has a similar or related nutritional explanation. The differences in distribution of infective disease found by these workers in the two tribes are most impressive. Thus in the cereal-eating tribe, bronchitis and pneumonia accounted for 31 per cent. of all cases of sickness, tropical ulcers for 33 per cent. and phthisis for 6 per cent. The corresponding figures for the meat, milk and raw blood tribe were 4 per cent., 3 per cent. and l per cent.

This is a problem that's more related to a low intake of animal foods and green vegetables than to grains per se.  Animal foods are a more effective source of vitamin A than plant foods, particularly in the subset of the population that converts plant carotenes into vitamin A inefficiently. 

Another issue is that grains are low in potassium compared with tubers.  Potassium is an important nutrient for bone and cardiovascular health, and insufficient intake (i.e. the amount most Westerners eat) may promote osteoporosis and hypertension (18, 19).  All else being equal, a diet based on tubers such as potatoes, sweet potatoes, or taro will be higher in potassium than one based on grains.

The point of all this is to show that we aren't yet well enough adapted to an agricultural diet that we can subsist primarily on a high-grain, very low animal food diet without facing health consequences, particularly if diet diversity is low.  If we had another million years of grain-heavy diets, we would likely be able to subsist on them more effectively, like rodents who are more able to access minerals from whole grains than humans (20).  That being said, this does not suggest that grains, including whole grains, cannot be part of a healthy diet in moderation.  To take that statement out of double negative land, in my opinion well prepared grains can be part of a healthy, diverse, omnivorous diet for most people, particularly if they're "externally digested" by fermentation.  Some people will benefit from avoiding wheat however, particularly flour.

Conclusion

It's time to wrap up this lengthy series.  I hope a few people followed along to the end.  The evidence suggests that many human populations have been rapidly evolving since the end of the Paleolithic, and that some of this evolving has made us better suited to consuming agricultural foods such as grains and dairy.  We aren't simply hunter-gatherers in a suit and tie-- we're an amalgam of hunter-gatherer and non-industrial agriculturalist adaptations, with a lot of population and individual variability.  The implication is that grains, dairy, and perhaps legumes are part of the European ancestral diet, stamped into our genome, and this applies to many other human lineages as well.  If these foods agree with you, in my opinion they can be part of a healthy diet in moderation.  However, some people are healthier and feel best when eating a stricter "Paleolithic" diet that excludes agricultural foods, and there is currently good evidence from controlled trials to support the health benefits of this dietary pattern in certain people, particularly those with glucose intolerance or diabetes (21, 22).