The fad for dietary adaptations is not going away

Food is a big deal for humans. Without it we die. Unlike some animals (here’s looking at you pandas) we’re omnivorous. We eat fruit, nuts, greens, meat, fish, and even fungus. Some of us even eat things which give off signals of being dangerous or unpalatable, whether it be hot sauce or lutefisk.

This ability to eat a wide variety of items is a human talent. Those who have put their cats on vegetarian diets know this. After a million or so years of being hunters and gatherers with a presumably varied diet for thousands and thousands of years most humans at any given time ate some form of grain based gruel. Though I am sympathetic to the argument that in terms of quality of life this was a detriment to median human well being, agriculture allowed our species to extract orders of magnitude more calories from a unit of land, though there were exceptions, such as in marine environments (more on this later).

Ergo, some scholars, most prominently Peter Bellwood, have argued that farming did not spread through cultural diffusion. Rather, farmers simply reproduced at much higher rates because of the efficiency of their lifestyle in comparison to that of hunter-gatherers. The latest research, using ancient DNA, broadly confirms this hypothesis. More precisely, it seems that cultural revolutions in the Holocene have shaped most of the genetic variation we see around us.

But genetic variation is not just a matter of genealogy. That is, the pattern of relationships, ancestor to descendent, and the extent of admixtures across lineages. Selection is also another parameter in evolutionary genetics. This can even have genome-wide impacts. It seems quite possible that current levels of Neanderthal ancestry are lower than might otherwise have been the case due to selection against functional variants derived from Neanderthals, which are less fitness against a modern human genetic background.

The importance of selection has long been known and explored. Sickle-cell anemia only exists because of balancing selection. Ancient DNA has revealed that many of the salient traits we associate with a given population, e.g., lactose tolerance or blue eyes, have undergone massive changes in population wide frequency over the last 10,000 years. Some of this is due to population replacement or admixture. But some of it is due to selection after the demographic events. To give a concrete example, the frequency of variants associated with blue eyes in modern Europeans dropped rapidly with the expansion of farmers from the Near East ~10,000 years ago, but has gradually increased over time until it is the modal allele in much of Northern Europe. Lactase persistence in contrast is not an ancient characteristic which has had its ups and downs, but something new that evolved due to the cultural shock of the adoption of dairy consumption by humans as adults. The region around lactase is one of the strongest signals of natural selection in the European genome, and ancient DNA confirms that the ubiquity of the lactase persistent allele is a very recent phenomenon.

But obviously lactase is not going to be the only target of selection in the human genome. Not only can humans eat many different things, but we change our portfolio of proportions rather quickly. In a Farewell to Alms the economic historian Gregory Clark observed that English peasants ate very differently before and after the Black Death. As any ecologist knows populations are resource constrained when they are near the carrying capacity, and England during the High Medieval period there was massive population growth due to gains in productivity (e.g., the moldboard plough) as well as intensification of farming and utilization of all the marginal land.

After the Black Death (which came in waves repeatedly) there was a massive population decline across much of Europe. Because institutions and practices were optimized toward maintaining a much higher population, European peasants lived a much better lifestyle after the population crash because the pie was being cut into far fewer pieces. In other words, centuries of life on the margins just scraping by did not mean that English peasants couldn’t live large when the times allowed for it. We were somewhat pre-adapted.

Our ability to eat a variety of items, and the constant varying of the proportions and kind of elements which go into our diet, mean that sciences like nutrition are very difficult. And, it also means that attempts to construct simple stories of adaptation and functional patterns from regions of the genome implicated in diet often fail. But with better analytic technologies (whole genome sequencing, large sample sizes) and some elbow grease some scientists are starting to get a better understanding.

A group of researchers at Cornell has been taking a closer look at the FADS genes over the past few years (as well as others at CTEG). These are three nearby genes, FADS1FADS2, and FADS3 (they probably underwent duplication). These genes are involved in the metabolization of fatty acids, and dietary regime turns out to have a major impact on variation around these loci.

The most recent paper out of the Cornell group, Dietary adaptation of FADS genes in Europe varied across time and geography:

Fatty acid desaturase (FADS) genes encode rate-limiting enzymes for the biosynthesis of omega-6 and omega-3 long-chain polyunsaturated fatty acids (LCPUFAs). This biosynthesis is essential for individuals subsisting on LCPUFA-poor diets (for example, plant-based). Positive selection on FADS genes has been reported in multiple populations, but its cause and pattern in Europeans remain unknown. Here we demonstrate, using ancient and modern DNA, that positive selection acted on the same FADS variants both before and after the advent of farming in Europe, but on opposite (that is, alternative) alleles. Recent selection in farmers also varied geographically, with the strongest signal in southern Europe. These varying selection patterns concur with anthropological evidence of varying diets, and with the association of farming-adaptive alleles with higher FADS1 expression and thus enhanced LCPUFA biosynthesis. Genome-wide association studies reveal that farming-adaptive alleles not only increase LCPUFAs, but also affect other lipid levels and protect against several inflammatory diseases.

The paper itself can be difficult to follow because they’re juggling many things in the air. First, they’re not just looking at variants (e.g., SNPs, indels, etc.), but also the haplotypes that the variants are embedded in. That is, the sequence of markers which define an association of variants which indicate descent from common genealogical ancestors. Because recombination can break apart associations one has to engage with care in historical reconstruction of the arc of selection due to a causal variant embedded in different haplotypes.

But the great thing about this paper is that in the case of Europe they can access ancient DNA. So they perform inferences utilizing whole genomes from many extant human populations, but also inspect change in allele frequency trajectories over time because of the density of the temporal transect. The figure to the left shows variants in both an empirical and modeling framework, and how they change in frequency over time.

In short, variants associated with higher LCPUFA synthesis actually decreased over time in Pleistocene Europe. This is similar to the dynamic you see in the Greenland Inuit. With the arrival of farmers the dynamic changes. Some of this is due to admixture/replacement, but some of it can not be accounted for admixture and replacement. In other words, there was selection for the variants which synthesize more LCPUFA.

This is not just limited to Europe. The authors refer to other publications which show that the frequency of alleles associated with LCPUFA production are high in places like South Asia, notable for a culture of preference for plant-based diets, as well as enforced by the reality that animal protein was in very short supply. In Europe they can look at ancient DNA because we have it, but the lesson here is probably general: alternative allelic variants are being whipsawed in frequency by protean shifts in human cultural modes of production.

In War Before Civilization Lawrence Keeley observed that after the arrival of agriculture in Northern Europe in a broad zone to the northwest of the continent, facing the Atlantic and North Sea, farming halted rather abruptly for centuries. Keeley then recounts evidence of organized conflict in between two populations across a “no man’s land.”

But why didn’t the farmers just roll over the old populations as they had elsewhere? Probably because they couldn’t. It is well known that marine regions can often support very high densities of humans engaged in a gathering lifestyle. Though not farmers, these peoples are often also not nomadic, and occupy areas as high density. The tribes of the Pacific Northwest, dependent upon salmon fisheries, are classic examples. Even today much of the Northern European maritime fringe relies on the sea. High density means they had enough numbers to resist the human wave of advance of farmers. At least for a time.

Just as cultural forms wane and wax, so do some of the underlying genetic variants. If you dig into the guts of this paper you see much of the variation dates to the out of Africa period. There were no great sweeps which expunged all variation (at least in general). Rather, just as our omnivorous tastes are protean and changeable, so the genetic variation changes over time and space in a difficult to reduce manner. The flux of lifestyle change is probably usually faster than biological evolution can respond, so variation reducing optimization can never complete its work.

The modern age of the study of natural selection in the human genome began around when A Map of Recent Positive Selection In the Human Genome was published. And it continues with methods like SDS, which indicate that selection operates to this day. Not a great surprise, but solidifying our intuitions. In the supplements to the above paper the authors indicate that the focal alleles that they are interrogating exhibit coefficients of selection around ~0.5% or so. This is rather appreciable. The fact that fixation has not occurred indicates in part that selection has reversed or halted, as they noted. But another aspect is that there are correlated responses; the FADS genes are implicated in many things, as the authors note in relation to inflammatory diseases. But I’m not sure that the selection effects of these are really large in any case. I bet there are more important things going on that we haven’t discovered or understood.

Obviously genome-wide analyses are going to continue for the foreseeable future. Ten years ago my late friend Mike McKweon predicted that at some point genomics was going to have be complemented by detailed follow up through bench-work. I’m not sure if we’re there yet, but there are only so many populations you can sequence, and only to a particular coverage to obtain any more information. Some selection sweeps will be simple stories with simple insights. But I suspect many more like FADS will be more complex, with the threads of the broader explanatory tapestry assembled publications by publication over time.

Citation: Ye, K., Gao, F., Wang, D., Bar-Yosef, O. & Keinan, A. Dietary adaptation of FADS genes in Europe varied across time and geography. Nat. Ecol. Evol. 1, 0167 (2017).

16 thoughts on “The fad for dietary adaptations is not going away

  1. But why didn’t the farmers just roll over the old populations as they had elsewhere? Probably because they couldn’t. It is well known that marine regions can often support very high densities of humans engaged in a gathering lifestyle. Though not farmers, these peoples are often also not nomadic, and occupy areas as high density.

    A tangentially related point: I suspect population high density was not the only major reason why maritime hunter(fisher)-gatherers were able to resist the larger farmer populations. Both hunting/fishing/gathering and pastoral nomadism confer two additional advantages as they relate to war. First, they build skills that translate to warfare much better than farming. Second, they are far less labor-intensive modes of production than farming, which leave more time for warring and war-practicing.

    It is for the same reasons why semi-nomadic populations on the fringes of civilization often terrorized and ruled over their nearby larger agricultural populations throughout history until the advent of gunpowder weapons. They possessed both the superior warmaking skillsets of nomadism AND enough population density made possible by living near, and trading with (and raiding against), high population density agricultural areas, to pose serious military threats to the latter.

    Moreover, until the advent of modern transportation, there was no such thing as supply trains (save ships). Armed men lived off the land they invaded (an average human can probably carry about three days worth of food on top of weapons and gear). Nomads (or semi-nomads) invading an agricultural civilization found plenty to eat and sustain themselves while the reverse was not the case.

  2. Your 5th sentence immediately prompted me to think of Fugu, said to be the only thing the Emperor of Japan is forbidden to eat. I once had a very enjoyable and informative conversation with an old Prof. of Toxicology (when we were in a maximum security prison together – just visiting, you understand) who had been to Japan specifically to try eating Fugu himself, to experience its effects, which he described for me.

    Living in a Chinese society, I have eaten some pretty weird things, but nothing on earth would persuade me to eat something where the skill of the chef is in leaving just enough of the toxin for you to experience the effects without actually dying from them.

  3. Re: Fugu

    It’s not just the emperor. The members of the inner imperial family are forbidden to eat it. But there are lots of prohibitions against dangerous activities for the Japanese imperial family.

    But Fugu is pretty safe. The final test for certified fugu chefs is to eat one’s own preparation. Most fail… and pay the price (rarely death, just a trip to the ER). Those who pass are highly skilled. And there are certified fugu chefs in the U.S. (that is, certified in Japan). I don’t know about Australia.

    By the way, Koreans also eat fugu (cooked) and have brought it to the U.S.:

  4. “But why didn’t the farmers just roll over the old populations as they had elsewhere?”

    The soil was just too difficult to plough in much of Northern Europe until the combination of skilled metallurgy and strong domesticated animals made it possible on a large scale.

    The deeply ice covered regions of the last glacial period are also the regions where farmers needed strong animals and metal ploughs to compete without seriously relying on hunting/fishing to supplement their diet.

    Although metals and draft animals allow you to make weapons and fight, they more importantly allow you to cut and turn difficult soil, cut trees, pull stumps, and remove large stones from fields (among countless other things).

  5. Is there any way to find out about my own variant for the FADS1 gene through my raw genome from 23andme? As a 20-year vegan I am curious. Though presumably if I didn’t have the “vegetarian” allele I would have had some significant health issues by now.

  6. I’ve had Fugu when I was in Japan. I went to Zubara-ya in Osaka for it, as part of attempt to try all the foods I can’t get in the West while in Japan (I skipped on whale meat because nearly everyone in Japan told me it was awful and hard to get; greasy and gross tasting). Fugu doesn’t have much in the way of flavor; and it’s also fairly tough when raw. It does have the interesting effect that your lips and tongue get mildly tingly when you eat it, either due to minuscule amounts of the poison, or placebo effect.

    Interestingly, folks have discovered that by restricting the diet of fugu fish, farm-grown fugu lack the neurotoxins of wild caught.

    You kind of wonder how people get around to figuring out things like Fugu or Cassava. “Hmmmm, I only got really sick. Didn’t die this time. How about I try preparing it this way, only more carefully?”

  7. Spike – similarly for some Australian Aboriginal plant foods that were toxic without quite complex (and non-intuitive) processing to render them non-toxic. The processing was done by women. I always got a mental picture of some woman trying random processes and testing the outcome on a series of unfortunate husbands until she hit on the right way to do it. But it can’t have happened that way, which leaves me with an unanswered (and probably unanswerable) question.

    The toxicologist I spoke to described similar symptoms from eating Fugu that you describe.

  8. BTW, if anyone lives in the Pacific Northwest or visits Seattle, the place for Fugu is Shiki:

    The owner, Ken Yamamoto, was certified in Japan for Fugu. I used to frequent his nondescript and modest restaurant back when I lived in the Pacific Northwest. An immigrant from Japan, was the head Sushi chef at the Westin in L.A. for a while before opening his own in Seattle years ago. Very funny and interesting guy. Was often seen atop his Harley outside the restaurant.

  9. You kind of wonder how people get around to figuring out things like Fugu or Cassava. “Hmmmm, I only got really sick. Didn’t die this time. How about I try preparing it this way, only more carefully?”

    If you are starved, you will eat anything. At the other end of the spectrum, elites in most societies often seek the exotic, including in food.

    Eating Fugu is probably A LOT less dangerous than many other activities, in which people routinely engage, such as rock climbing, mountain bicycling, surfing, scuba diving, hard contact sports, hunting, etc. Or for that matter, drinking untreated water or “fresh” food in many parts of the world.

  10. “Both hunting/fishing/gathering and pastoral nomadism confer two additional advantages as they relate to war (…) Second, they are far less labor-intensive modes of production than farming”

    I am not sure if fishing is really less labor-intensive than farming – at least some cultures, like wheat, require almost no labor during many mounths.

    “Eating Fugu is probably A LOT less dangerous than many other activities”

    This is today; but in the history of Fugu, surely it was a time when people did not know how to prepare the fish and probably it required much try-and-error (try-and-death) to discover the correct way of cooking it. The question is why, even usually dying of eating fugu, people continued trying to discover a safe way of prepare fugu, instead of simply assuming that it was poisonous and abandoning it.

  11. Isn’t feeding cats a vegetarian diet dangerous (by ‘vegetarian’ I mean no animal flesh whatsoever; I suppose cats can survive on fish and chicken even without red meat) because they need an element (taurine, I believe) that is only found in animal products and without which they can go blind?

  12. At least, I should say, vegan is. Vegetarian, if it includes eggs and milk, I don’t know about. But some crazies put their cats on vegan diets and wonder why they die.

  13. Karl,

    You can search the 23andme raw data for specific genes or SNPs and it will give you any variants it detected. Comparing it to the paper Razib linked I found information for rs174546, rs174570,rs2851682 for myself.

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