BAF60c: Hero or villain?

UC Berkeley researchers have identified the gene that flashes dietary carbohydrate into body fat: BAF60c. http://newscenter.berkeley.edu/2012/12/06/gene-converts-carbs-to-fat/. When mice had this gene disabled, no matter how they gorged on carbohydrates, they stayed sleek and svelte, while those with enhanced BAF60c continued pumping out fat storage genes even when fasting. I’ll be asking Dr. Sul, some questions about this gene!

 

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Adam or Eve?

In my previous post, I said that a favourable mutation (in this case for increased fat deposition) in even one woman, in a very small population group such as those that occurred during the Middle Stone Age, would be fixed very rapidly – and suddenly had a thought that  I was taking it for granted that this mutation occurred in a woman when it might very well have occurred in a man! However, upon thinking it through, I am inclined to conclude that an African Eve, rather than an Adam, got the lucky roll of the genetic dice, for these reasons:

1. Women have two X chromosomes, one from each parent, while men have one X and one Y. Both sons and daughters get their X chromosome from their mother, who cannot contribute anything else. Daughters get an X and sons a Y from their father.

2. Women, across cultures, carry almost twice as much fat as men, even when matched for age, height, ethnicity, and weight.

3. This looks to me as if women have two copies of the fat-depositing gene, one on each X chromosome.

A woman would pass on the adiposity genes in an equal-opportunity fashion, to both sons and daughters, who would then disseminate it very rapidly. A man undergoing such a mutation affecting his X-chromosome would pass on the gene only to his daughters, and were the gene located on his Y-chromosome would pass it on only to his sons. While the daughters would pass it on to their sons, who would again pass it on to their daughters, and so on in perpetuity, my hunch is that there would then be little or no sexual dimorphism in fatness.

Over time, it’s possible that some individuals may have developed multiple copies of this adiposity gene, just as Asians have many more copies of the gene influencing amylase expression, making them better able to metabolize starches. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2377015/

The paper linked above, Diet and the evolution of human amylase gene copy number variation, by Perry et al, 2007, notes that freeliving wild born chimpanzees have only 2 diploid copies of the AMY1 gene, which influences starch digestion, while even humans with a low number have 6. To me, this suggests that the initial mutation may have occurred during crossingover in meiosis, such that some lucky individual got an extra allowance of AMY1, allowing her to better digest starch and lay down fat. As daughter populations hived off and some underwent selective pressure through environmental determinism pushing their diet to starch as a staple, extra copies might then be generated.

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Minding the gap

I think I can narrow the timespan – if anatomically modern humans, in the Out of Africa II scenario, left their mother continent around 60,000 years ago, the ability to lay down fat would likely have been fully functional by then. This is getting exciting – it looks now to me as if we Scatterlings of Africa started getting plump between 75,000 and 60,000 years ago. With a small bottleneck population, of which an even smaller number would be nubile females, a favourable mutation in even one woman could be very rapidly fixed!

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Boom or Bust In The Middle Palaeolithic

Doubtless readers of my blog have noticed a serious hole in my process: where, you might well ask, is the evidence that anatomically modern human populations suddenly started to grow in the Middle Palaeolithic? All my other work has baked a nice big fluffy bun, but where’s the beef? https://www.youtube.com/watch?v=Ug75diEyiA0

In an earlier post “Always Something New”, I cited Sarah Blaffer Hrdy to this effect, but have not, until now, brought any heavy guns to bear. Duck, cover, and hold, because the big artillery has arrived!

Here’s a pretty graph from the University of Michigan:

http://www.globalchange.umich.edu/globalchange2/current/lectures/human_pop/human_pop.html

Note, there is a quantitative leap sometime before 10,000 years ago, shown by the insertion of a new line segment disconnected from the previous segment. The broad time scale, and inevitable drawing of the eye to the much more impressive population numbers and gains of our recent history make this little blip seem insignificant, yet it is the turning point for our species. The associated gains in cultural evolution have gotten the kudos for our subsequent success, but as Brown & Konner pointed out, we are unique among living creatures because our evolutionary engine has two pistons: culture and biology (29).

Heavy gun #1: Mary C. Stiner, Natalie D. Munro, Todd A. Surovell, Eitan Tchernov, & Ofer Bar-Yosef (2009), in their paper Paleolithic Population Growth Pulses Evidenced by Small Animal Exploitation, analyzed the proportions of small and large prey remains in dietary assemblages. Small prey proportions, they say, “are more sensitive indicators of the changes in human population density because small prey species vary much more than ungulate species with respect to life history and predator avoidance characteristics.” They conclude that early Middle Palaeolithic human populations were “exceptionally small and highly dispersed” and that population densities “increased abruptly during the late Middle Paleolithic and again during the Upper and EpiPaleolithic periods.”

While I am concentrating my attention on the first of these periods, it is compelling that the second part of the Paleolithic saw the appearance of the Venuses, AND a greater reliance on grains and pulses (carbohydrates) in the plant fraction of the diet (Maher 2012).

To me it looks like this: Once the thrifty gene/phenotype had been acquired, it was rapidly fixed and came without brakes: we raced from gaining significant fat, highly adaptive for survival and breeding success, to obesity as we incorporated more starches and sugars into our daily diets. While pulses are usually thought of as high-protein foods, they are also rich in starch and sugar.

Heavy Gun #2: Stanley Ambrose’s 1998 paper, Late Pleistocene human population bottlenecks, volcanic winter, and differentiation of modern humans, explores reasons for the genetic bottleneck and release affecting anatomically modern humans around and after the time of the Mt. Toba eruption. He says, “Around 50ka, dramatic growth occurred within dispersed populations that were genetically isolated from each other. Population growth began earliest in Africa and later in Eurasia …”The reason for this, he says, is usually ascribed to better technology, “which developed in equatorial Africa” (623). Stanley then goes on to suggest that bottleneck/release mechanisms may be driven by factors of climate and geography.

Heavy gun #3: David E. Reich and David E. Goldstein (1998) delved into the genes of aboriginal populations worldwide. The results of running statistical tests on a number of genetic markers: a major population expansion occurred in Africa but nowhere else (paper abstract), sometime between 44,000 and 570,000 years ago (see correction to paper).

These three lines of evidence – archaeological, climatic/geographical, and genetic – support the hypothesis that there was a sudden surge in anatomically modern human populations, in Africa, during the Middle Paleolithic. Note: climate alone is unlikely to have driven this, as sapiens had previously enjoyed 50,000 years of warm wet weather without concomitant expansion in population size, and the cold dry interval appears to have killed us off in the Levant. After our return to the Levant, it seems that succeeding cold dry intervals had lost their biological power over us; secure in our fatty envelopes, we simply tweaked our technology and social coping skills.

Ambrose, Stanley. Late Pleistocene human population bottlenecks, volcanic winter, and differentiation of modern humans. 1998. Journal of Human Evolution 34:623-651.

Brown, Peter J. and Melvin Konner. An anthropological perspective on obesity. 2006. Annals of the New York Academy of Sciences 499: 29-46

Hrdy, Sarah Blaffer. 1999. Mother Nature: a history of mothers, infants, and natural selection. Pantheon Books, Random House, Inc., New York, N.Y.

Reich, David E. and David B. Goldstein. Genetic evidence for a Paleolithic human population expansion in Africa. 1998. Proceedings of the National Academy of Sciences, USA. 95:8119-8123.

Stiner, Mary C., Natalie D. Munro, Todd A. Surovell, Eitan Tchernov, & Ofer Bar-Yosef. Paleolithic population growth pulses evidenced by small animal exploitation. 1999. Science 283:190-194.

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From African Eve to European Venus

Unfortunately there is little art from any period before the Upper Palaeolithic, so it isn’t possible to compare and contrast imagery to either refute or support my contention that the ability to fatten was gained late in our evolutionary history.

The Venus of Tan-Tan, from Morocco, if indeed it is a hominin-modified pebble and not a natural pebble, is too old for our species to have made it, as it is 500-300kya.

It may have been painted with red ochre, which would make it an artifact regardless of whether the shape is entirely natural. Image and information: http://en.wikipedia.org/wiki/Venus_of_Tan-Tan. If this is an artifact, it would have been made by H. erectus or H. heidelbergensis.  My take: is it intended to be female? It looks fairly phallic!

 Venus of Berekhet Ram: Found in the Golan Heights,  Israel (Levant), around 280,000-250,000 years old.

Alexander Marshack has intensively studied this object, and concludes on the basis of scanning electron micrographs that it was deliberately modified using flint tools to increase its resemblance to that of a robust female (Marshack 1997:). Again, there is a problem with the age: the figurine must have been made by H. neandertalensis  or a non-anatomically modern sapiens. She is definitely chunky, but it looks like heavy bone and solid muscle (small breasts, flat belly), and there’s no way to measure her body fat %.

Our oldest depictions of anatomically modern women all come from Europe – but we are all Africans anyway. From left to right: the Venus of Hohle Fels, Germany, 40-35kya, mammoth ivory; the Venus of Galgenburg, Austria, 30kya, serpentine; and the Venus of Dolni Vestonice, Czech Republic, 31-27kya, ceramic. All images from Wikipedia.

There has been a good deal of argument about whether these figurines represent real women or the yearnings of a population whose women are trapped in skinny bodies. On the side of the dreamgirl theorists is Eric Colman, M.D., whose 1998 paper, “Obesity in the Palaeolithic Era? The Venus of Willendorf” outright dismisses any possibility of obesity but is willing to consider Cushing’s syndrome. He argues that seeing hunter-gatherers were not sedentary and because their diet was lower in fat than that of today, nobody could have been other than lean and muscular. As this is his starting point, his conclusion is inevitable: “Obviously, we will never know exactly what inspired the creation of the Venus of Willendorf, nor will we know its true meaning. Nevertheless, this ancient work of art serves as a valuable reminder that obesity is a disease unique to the modern world and one in which environmental factors, such as diet and exercise, assume critical etiologic roles.”

Hmm. There’s a fair amount of circularity to this argument: Paleo people got a lot of exercise and ate a low fat diet, hence they could not be obese, hence the Venus is not drawn from life, hence obesity is a modern disease and looking at the Venus should drive us to high exercise, low fat diet living. Hmmm.

Another medical doctor, the practising gynaecologist Jean-Pierre Duhard, is equally certain that he knows what’s what. In the course of his work, Duhard has seen many naked women, and he says that modern women exhibit the same range of shapes and sizes as the Venuses. He backs up his contention with a plate of line drawings of modern women, below (554). Like Colman, he recognizes some medical conditions. However, Duhard’s conclusion is that Palaeo artists were simply working from life and producing portraits (1991:559).

Finally, Katheryn C. Twiss, in discussing the Neolithic of the southern Levant, includes this image (2007:27). Although stylized, the female figures are of physical types recognizable to any modern woman who looks around the locker room at the gym, and they have goodly fat deposits. The figures range from around 11,700 to 9,000 years old.

While I haven’t proved beyond reasonable doubt that humans, especially women, first acquired their modern ability to store large amounts of body fat during the Middle Palaeolithic, I think there is good reason to suspect this, given that normal fatness is strongly correlated with reproductive fitness, and that there was an uptick in our breeding rate when we recolonized the Levant. We exhibited a cultural blossoming on our return, and it seems that we acquired a full suite of anatomically modern behaviours during the critical period, 75-45kya, that we were gone from the Levant but present in Africa. It seems very likely to me that that our cultural evolution event was conjoined to a biological evolution event involving fattening.

I’m giving the last word to Johnny Clegg and Savuka: we are all “Scatterlings of Africa.”

Colman, Eric. 1998. Obesity in the Paleolithic Era? The Venus of Willendorf. Endocrine Practice. Vol. 4. No. 1. 58-9.

Duhard, Jean-Pierre. 1991. The shape of Pleistocene women. Antiquity 65:552-61

Twiss, K. C. 2007. The Neolithic of the southern Levant. Evolutionary Anthropology, 16, 24-35.

Wikipedia: The Venus of Tan-Tan. http://en.wikipedia.org/wiki/Venus_of_Tan-Tan
                    The Venus of Berekhat Ram. http://en.wikipedia.org/wiki/Venus_of_Berekhat_Ram
                    The Venus of Hohle Fels. http://en.wikipedia.org/wiki/Venus_of_Hohle_Fels
                    The Venus of Galgenburg. http://en.wikipedia.org/wiki/Venus_of_Galgenberg
                    The Venus of Dolni Vestonice. http://en.wikipedia.org/wiki/Venus_of_Doln%C3%AD_V%C4%9Bstonice

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Always Something New

When Pliny the Elder commented, Ex Africa semper aliquid novi, (Out of Africa always something new), in 79AD, he was talking of African animals, and he was quoting Aristotle’s book on natural history, written 2,300 B.C. (Mayell, 2003)

Archaeologists could well make the same remark, in reference to just one animal: Homo. Africa, at each throw of the genetic dice, turned up hominin after hominin until it came to us – but the party didn’t stop with the first anatomically modern humans around 195 kya at Omo Kibish and Herto, Ethiopia. It was in Africa, as McBrearty and Brooks, showed in their paper The Revolution That Wasn’t, published 2000, that each single component of fully modern human behaviour evolved, whether harpoon, microlith and compound tool, or symbolic expression through hatching of ochre. I argue that during this same period, the Middle Palaeolithic, anatomically modern humans, H. sapiens, evolved a cunning new biological twist to accompany all this cunning new cultural stuff. I think that during the Middle Palaeolithic Africa dialed up our potential to lay down astounding amounts of body fat, which in turn led to increased survivability in the Levant and Eurasia after recovery from the H5 Heinrich Event.

We humans are fat, fat, fat, even when we’re skinny, compared to other primates and even to other mammals. In my earlier post, The Fats of Life, I concluded that our fattiness, and high sexual dimorphism in body fat percentage, must confer an adaptive advantage, and I’ve presented evidence that reproduction costs bear very heavily on women, who use this fat to fuel pregnancy and lactation.

There’s little evidence to show when this fattening ability came into our lineage; Leslie Aiello et al suggest that the tendency arose during the Homo erectus period, when there was a sudden increase in our body size (2002: 552). It was in this period that we probably started cooking, grew our brain, and shrank our gut. We may also have started talking at this time, and we may have lost our fur then. Caroline Pond presents evidence that other primates, notably the orangutan, have some ability to pack a paunch. Other plump animals lay down their fat along the back, which is why farmers pinch their cattle and sheep around the root of the tail to assess their condition. Only primates lay down their fat in front – Pond suggests that it may be a form of sexual signalling indicating good body condition. For primates, the belly is often on view so we can strut our stuff effortlessly (Pond 1998: 42-45).

My point: we were probably preadapted to fattening under the right conditions. I argue that these conditions arose in East Africa during the Middle Palaeolithic while Neandertals ruled the Levant and then disappeared into the dust of eternity: between 75 and 50 kya. I’m picking on East Africa because it’s almost certainly the birthplace of hominids, hominins, and H. sapiens.

This table is adapted from information provided in my Anthropology 128 class, Fall 2012, by Professor Lisa Maher.

Later sapiens could well have recolonized the Levant from East Africa, and the difference in behaviour and economy after only 30,000 years, a blink in our evolution, is striking. Something was going on during Marine Isotope Stage 4 that catapulted us into a new paradigm.

What was happening in East Africa during MIS 4?

While the degree of the effects of the Mount Toba supervolcano eruption are debated, there is consensus that a 6-10 year volcanic winter set in that affected the entire world, lowering average temperature, and probably reducing the amount of sunlight that reached Earth’s surface because of gigantic ash clouds and emission of aerosol gases. (Wikipedia: Toba)  East Africa, however, was probably buffered from the worst effects, becoming somewhat colder and drier, but not as markedly as the Levant (Maher 2012). Also, its position on the Equator would maximize its solar gain. However, less light and less water would have borne hardly on forests, so grasslands would have expanded as forests shrank.

Another point in its favour: East Africa does not have the geographic circumscription of habitable zones characteristic of the Levant. Humans would have been able to migrate, following the food, whether plant or animal, as well as exploit both forest and grassland. However, game herds may well have shrunk during this time, in lockstep with the diminishing productivity of the plants on which they feed, forcing humans to start exploiting their environment more intensively.

Small fast prey like rabbits and birds need different hunting weaponry, and new technology might well be needed to extract the maximum nourishment from plant foods. Tubers or seeds might need to be crushed or pounded, knives might be in demand for peeling and slicing, and perhaps new cooking methods might have to be devised. Of interest in this regard is the finding of Phillipson et al. that “the heavily worn grindstones” found in the Nile Valley had been used to process the tubers of Cyperus rotundus, commonly known as wild nutgrass , thus warning against the assumption that grindstones equal grain (147, 148). According to Wikipedia, these 1″ long tubers are somewhat bitter, but edible, and are very rich in minerals and vitamins. They also have medicinal properties (Wikipedia: Cyperus rotundus).

Necessity is the mother of invention: with the rapid onset of bad climate (within 3 years of the Mount Toba explosion, according to the Wikipedia article referenced above), humans, particularly women, would have had to turn to other foods. Leaves and fruits were scarcer. What’s a hungry human to eat? What about tubers?

Freeliving chimpanzees, who make digging tools to grub them out, eat tubers (Kiderra 2007).  The great Bob Brain claims that australopithecines were routinely extracting tubers at Swartkrans, South Africa, around 1 million years ago (Vincent 1985:131). For some nice pictures of this famous site:  http://swartkrans.org/history-of-swartkrans/. Probably humans have been eating tubers all along. Forests are not prolific tuber producers; in Tanzania, forest produces 0.5 tonnes-hectare of tubers, while savanna produces a bounty of edible bulbs – ranging from 5 – 2,000 tonnes/hectare, depending on species and local conditions, with only pigs and porcupines as competitors. These bulbs can be eaten raw as well as cooked, unlike grains. Anne Vincent, whose work I am citing here, says that one hectare of savanna produces enough tubers to feed three families for 148 days (1985: 139). Tubers are more reliable than grains, and can be left underground until needed, without deterioration in quality, while they regenerate faster than cereals.

Tubers are a rich source of carbohydrate, with varying proportions of starch and sugar. Gary Taubes, in his intensively researched book Good Calories, Bad Calories, argues persuasively that the prime driver of fat deposition is carbohydrate (see summary p454). This is certainly in line with the work of Leslie Aiello and Jonathan C.K. Wells, who show that humans can metabolize only enough lean meat to meet half of their daily requirements (2002: 326), and with that of John D. Speth and Katherine E. Spielmann, who discuss the   phenomenon of rabbit starvation, where tribes forced to eat lean meat as a staple, although having more than enough calories can essentially starve to death (1982: 3,4), and find that carbohydrate is non-replaceable by fat when it comes to protein sparing and muscle maintenance (6,7). Without sufficient body fat, calcium is not properly metabolised and essential vitamins are not stored (17,18).

Returning to Vincent’s work, women gathering tubers have full control of the resource, and they often eat a considerable amount of what they gather in situ. The same is true of berries and fruit . The high-status foods, meat and honey, are obtained and controlled by men, who share them out according to the societal norms (1985:135). It seems probable that natural selection would favour women able to rapidly fatten on a high-carbohydrate diet, as they would reach menarche earlier (Frisch 1990; Guo 2011), be more likely to retain a pregnancy to full term, and successfully lactate for 3 – 4 years, thus weaning a child more likely to survive till puberty.

One last tempting titbit: Sarah Blaffer Hrdy says that at the beginning of the Palaeolithic our species doubled its population size only every 15,000 years. Then, starting with a single small band of hunter-gatherers sometime around 100,000 years ago, we became “newly fecund“ and the brakes came off the breeding train (1999:184). Could the reason be a thrifty gene or thrifty phenotype that allowed carbohydrate-eating women to get fat and get fertile?

Aiello, Leslie C. and Jonathan C.K. Wells. 2002. Energetics and the Evolution of the Genus Homo. Annual Review Anthropology. 31:323-38.

Frisch, Rose E. 1987. Body fat, menarche, fitness and fertility. Human Reproduction vol 2. No 6. 521-533.

Guo, Xiao Yan & J.I. Chenge Ye. 2011. Earlier menarche can be an indicator of more body fat: study of sexual development and waist circumference in Chinese girls. Biomedical and Environmental Science, 24(5). 451-458.

Hrdy, Sarah Blaffer. 1999. Mother Nature: a history of mothers, infants, and natural selection. Pantheon Books, Random House, Inc., New York, N.Y.

Kiderra, Inga. “Chimps Dig Up Clues to Human Past?” 12 November 2007. UC San Diego News Center. Accessed 7 November 2012. http://ucsdnews.ucsd.edu/newsrel/soc/11-07ChimpsDigCluesToHumanPastIK-I.asp

Maher, Lisa. 2012. Anthropology 128, Fall semester, University of California, Berkeley, USA. Class lecture notes.

Mayell, Hillary. “Out of Africa” Phrase in Use Since Ancient Greece.”  19 February 2003. National Geographic News. 7 November 2012. http://news.nationalgeographic.com/news/2003/02/0219_030219_outofafrica.html

McBrearty, S. & Brooks, A. S. 2000. The revolution that wasn’t: a new interpretation of the origin of modern human behavior. Journal of Human Evolution, 39, 453-563.

Phillipson, D. 2009. African Archaeology, Cambridge, Cambridge University Press. Chapters 4-5.

Pond, Caroline. 1998. The Fats of Life. Cambridge University Press, Cambridge, United Kingdom.

Speth, John D. & Katherine A. Spielmann. 1983. Energy source, protein metabolism, and hunter-gatherer subsistence strategies. Journal of Anthropological Archaeology, 2:1-31.

Taubes, Gary. 2007. Good Calories, Bad Calories. Alfred A. Knopf, New York, N.Y.

Vincent, Anne S. 1985. A preliminary report of tubers eaten by the Hadza of northern Tanzania. World Archaeology, 17(2):131-148.

Wikipedia. “Cyperus rotundus.” Last updated 28 October 2012. Wiki entry. Accessed 7 November 2012. http://en.wikipedia.org/wiki/Cyperus_rotundus

Wikipedia. Toba catastrophe theory. Last updated 23 October 2012. Wiki entry. Accessed 7 November 2012. http://en.wikipedia.org/wiki/Toba_catastrophe_theory

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Say It Again

Given the potential importance of Pontzer et al’s paper on hunter-gatherer energetics, I checked my table, corrected some arithmetical errors, and added a line for kg of body fat.

Then I made a graph.

This makes things clearer.

The data points are in the same order as Table 1: Hadza women and men, Western women and men, Bolivian farmer women and men. The data now reveal, in terms of energy output per kg of body mass per day, apparently marked differences between hunter-gatherers and farmers on the one hand, and Westerners on the other.

While the differences even out somewhat in terms of lean body mass for hunter-gatherers and Westerners and farming men, farming women are still way out there.

However, I still don’t see the point of working with lean body mass, given that fat is by no means inert and given that even lean people have a large amount of fat.

Further points to consider:

1. Energy output was measured at rest. Subjects sat quietly while breathing into apparatus that measured resting metabolic rate, from which basal metabolic rate was then estimated. For pregnant and lactating women, this may not be a good way to estimate total energy expenditure, as it does not take into account the increased difficulty of movement as pregnancy progresses – each task takes longer and is more awkward,and the throwing out of whack of normal balance by the increasing size of the belly in itself requires more energy to keep the woman upright. This increased energy usage is unlikely to show up while she is sitting peacefully.

2. While a lactating woman may not show increased energy output either while sitting or while walking, this may be because the cost of producing milk is being cancelled out by the simultaneous release of energy from her fat stores, which would probably not show up through the doubly-labelled water measurements as the fat was laid down long before the event. Hence, all that’s visible is her standard cost of metabolism and transport.

Women use fat from their body stores to support lactation, and they preferentially use fat from specific depots – the thighs, and the region called hips by Americans and buttocks by many others – which store considerably more DHA than any other female fat depot. Mark’s Daily Apple has a post stuffed with fascinating factoids about fat, his and hers, over here: http://www.marksdailyapple.com/gender-differences-in-fat-metabolism/#axzz2BAZaBjMg

In the pipeline: my reasons for arguing that the cultural evolution taking place in Africa during the Middle Pleistocene were accompanied by a biological evolution event affecting the ability of anatomically modern humans (us) to accrete large amounts of body fat.

Pontzer, Herman, David A. Raichlen, Brian M. Wood, Audax Z. P. Mabulla, Susan B. Racette, Frank W. Marlowe. 2012. Hunter-Gatherer Energetics and Human Obesity.
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0040503

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Say It Is Not So!!

Professor Maher sent me the paper linked below (thanks, Professor), which caused me a sinking of the heart when I realized that, if true, this research could completely sink my contention that women are fat because they need the stored energy to provide for pregnancy and lactation when times are lean. However, things are not nearly as bad as I feared!

Hunter-Gatherer Energetics and Human Obesity
Herman Pontzer, David A. Raichlen, Brian M. Wood, Audax Z. P. Mabulla, Susan B. Racette, Frank W. Marlowe
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0040503

Abstract

Western lifestyles differ markedly from those of our hunter-gatherer ancestors, and these differences in diet and activity level are often implicated in the global obesity pandemic. However, few physiological data for hunter-gatherer populations are available to test these models of obesity. In this study, we used the doubly-labeled water method to measure total daily energy expenditure (kCal/day) in Hadza hunter-gatherers to test whether foragers expend more energy each day than their Western counterparts. As expected, physical activity level, PAL, was greater among Hadza foragers than among Westerners. Nonetheless, average daily energy expenditure of traditional Hadza foragers was no different than that of Westerners after controlling for body size. The metabolic cost of walking (kcal kg−1 m−1) and resting (kcal kg−1 s−1) were also similar among Hadza and Western groups. The similarity in metabolic rates across a broad range of cultures challenges current models of obesity suggesting that Western lifestyles lead to decreased energy expenditure. We hypothesize that human daily energy expenditure may be an evolved physiological trait largely independent of cultural differences.

It certainly is a startling thesis statement: that all humans burn about the same amount of energy, give or take a standard deviation or two, regardless of whether we hunch over a hot keyboard all day, trudge under the African sun for many miles, or plant potatoes by hand on a high-altitude farm. This could certainly have put a stop to my slithering with my contention that humans are successful because they, especially the women, evolved a capacity to store fat. As I read the paper, however, I found a couple of questions burning at the back of my mind as I read, so I went back to the beginning and looked more closely. I don’t yet understand how doubly-labelled water is used to measure energy, but I can do arithmetic, so that’s what I did!

In Table 1, the researchers present their computations for Total Energy Expenditure per day, for Hadza hunter-gatherers, Westerners, and Bolivian farmers. They measured body mass, body fat percentage, and BMI, for each population.

Image

Pontzer et al., p 2.

It struck me – and the researchers noted this – that both the Hadza and the Bolivian farmers are considerably smaller than the Westerners. It seemed to me that energy expenditure per kilogram might be an interesting variable to consider rather than a blanket figure. So I sat down and worked out the TEE/kg of body mass for each group. Suddenly the picture changed, with a U curve appearing – see my table below.  Note that the Hadza and Bolivian men use much the same amount of energy/kg BM, and considerably more than Western men, while Hadza women use less than Bolivians, and both use considerably more than Western women. If a Hadza woman is scaled up to the same weight as a Western woman, she would use 3217.8 kCal/day -870.8, or 2.42 standard deviations more, which is statistically significant. A Western woman scaled to Bolivian size would use 1517.55 kCal/day; a difference of 951.45 kCal LESS At 3.02 standard deviations, this is statistically significant.

Hadza Western Farmers
Women Men Women Men Women Men
Mass (BM) kg 43.4 50.9 74.4 81.0 48.1 54.7
BF % 20.9 13.5 37.9 22.5 27.3 16
Lean BM (LBM)

BM – BF

34.3 45.9 46.2 62.8 34.9 45.9
TEE/kCal/day 1877 2649 2347 3053 2469 2855
TEE/kgMass/day 43.25 52.04 31.55 37.69 51.33 52.19
TEE/kg LBM 54.68 57.74 50.8 48.63 70.6 68.13

For the purposes of this quick-and-dirty analysis, I worked with average Body Mass, Body Fat, and Total Energy Expenditure.

Then I looked at TEE/kg lean body mass (I simply subtracted the body fat), and while the gap narrows between the Hadza and Westerners, the energy expenditure of the farmers goes way up, markedly widening the gap. However, I don’t think one should discard the fat, as while fat stores burn fewer calories per pound than muscle or brain or gut, even lean people have a fair number of pounds of fat! Further, the lean body mass includes bones, skin, gut, brain and muscle, each of which has varying energy needs. Hence, the energy needs of the whole organism, per kg body mass, seem to me to be a reasonable measure.

I found myself wondering how the energy needs were ascertained, and discovered that it was by calculation; the participants were asked to walk on a flat track, wearing ordinary clothes and sandals, at slow, medium, and fast paces set by a researcher walking alongside. The subject was wired up and energy usage measurements taken. The measurements taken were then multiplied by the average number of miles walked per day by Hadza men and women. The researchers admit that, as the Hadza walk over varied terrain at varied pace, Hadza energy output could be higher than the calculation.

Another thing that struck me was that there was no reference to burdened weight. A woman setting off on a foraging trip carries a fair load – she may have a baby in a sling or a toddler on her hip; if the latter, she may be pregnant. She’s probably carrying a container of water and some food; digging sticks and something with which to sharpen them (probably a panga), and a kaross or bag for the gathered food. On the way home, she’ll probably refill the water container, and she’ll be carrying many pounds of tubers, roots, and fruits, as well as the youngster, digging sticks, and panga. Atop this (literally), she probably collects firewood on her way home, bundling it onto her head.

Image

Figure 1. Hadza women in the field. http://acoach4u.com/life_coach_gallery.htm Note children being carried, and bulging food collecting slings.

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Figure 2. Hadza woman in harsher environment – note child on back, knotted sarong carrying food, panga. http://www.sciencedaily.com/releases/2012/01/120125132610.htm

Sarah Blaffer Hrdy, Mother Nature, p 198, describes a San woman’s foraging trip: in the last stages of pregnancy, she is carrying a 30lb 4 year old on her shoulders. Her kaross holds about 25lb of gathered food. Her personal belongings weigh another 5lb. She is carrying 60lb of weight outside her body plus the pregnancy weight. Anne Vincent, describing the use of tubers by Hadza women, photodocumented a woman loading her carrying sling with 20kg of tubers to carry home (1985: 138).

From my own experience, the physical changes of the last stages of pregnancy – the bulging belly, change in balance, and softening of the ligaments of the pelvic girdle, make walking more difficult and more tiring. When these factors are figured in, it would be surprising if the TEE for the day were not considerably higher than that calculated by Pontzer et al.

A man on his way to hunt is probably carrying a spear and thrower, or bow and arrows; he may also carry water and snacks. On his way home, he could be carrying a prey animal or several pounds of honey.

To me, it looks as if the energy needs of women in premodern societies are way higher than those of moderns, so much higher that stores of body fat are vital if the longterm reproductive success of the population through protracted periods of food shortages is to be assured.

Even if I am wrong in my basic assumptions here and Pontzer et al really have identified a stable energy output, and even if there really is no difference in energy output for pregnant and lactating women compared to women who are not pregnant or lactating, the role of maternal fat stores in transferring lipids to the infant (see The Fats of Life post) does not collapse and my hypothesis is not hopeless.

Hrdy, Sarah Blaffer. 1999. Mother Nature: a history of mothers, infants, and natural selection. Pantheon Books, Random House, Inc., New York, N.Y.

Vincent, Anne S. 1985. A preliminary report of tubers eaten by the Hadza of northern Tanzania. World Archaeology, 17(2):131-148.

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The Fats of Life

The Fats of Life

This clever title is that of a book by Caroline Pond, which I cannot recommend too highly to anybody interested in the vexed questions of dietary and body fat, especially from an evolutionary and functional viewpoint. I’m going to hit the high points from the viewpoint of my thesis question of how having plentiful body fat might ensure the success of our species through meeting its reproductive costs -which of course bear most heavily on women.

Pond says that we are among the fattest of all mammals, having ten times as many fat cells as would be expected for an animal of our size, more than “even notorious fatties like hedgehogs, bears, seals, and pigs” (51). Now this is interesting, because we don’t hibernate like hedgehogs and bears, and we don’t need massive insulation against cold like seals. Pigs, now, are generalist feeders like ourselves; indeed their internal systems are so like ours that pigs can be (and were, for a very long time) used to teach human internal anatomy. Wild pigs, like hunter-gatherers, are subject to seasonal variations and shortages in food, as well as feast-and-famine cycles. Pond concludes from her comparisons of populations of selected species that the fattest are always the populations whose food supply has the most fluctuations (pages 63-71). Pond says, page 232, that !Kung HGS lose 1-2% of their body mass every dry season, which she doesn’t regard as serious compared to the body mass fluctuations of, say, polar bears, whose late pregnancies and early lactations are supplied purely from body fat. However, what if dry season is followed by dry season? How long till body fat is depleted to the point where nobody’s getting pregnant any more, or able to successfully suckle a child? Hmmm.

More from Pond: obese humans are healthier than genetically obese non-humans (62) and humans do not fatten rapidly or efficiently when compared to birds, bears, or seal pups (232).

Pond says also that even apparently very thin people have just as many adipocytes as the obese; the difference lies in the size of the fat cells, not their number (51); this helps to explain why some thin young women have sizeable areas of ripply cellulite where they wish they didn’t.

I’ve shamelessly purloined Pond’s graph, (49), showing humans considerably above the line of best fit for body fat among several genera.

 

Humans, says Pond, have around 15% dissectible adipose tissue if they’re LEAN young men, while LEAN young women have 17-25%, but apparently lean people can still have over 30% dissectible adipose tissue, while most wild nonhuman animals run between 4-8% fat when living under “ideal nutritional conditions”(61); bolding added for emphasis.

Combined with the stuff I’ve already looked at, this strongly reinforces the suggestion that high body fat, especially for women, is highly adaptive and results from strong selective processes. But what do pregnant and nursing women do with all that fat?

  1. They stay pregnant.
  2. They transfer lipids to the baby
    First trimester: Build brain and nervous system
    Second trimester: build up baby’s fat stores
  3. They store and transfer fat-soluble vitamins
  4. They build up the infant’s immune system

1. They stay pregnant. We know already that the first trimester of pregnancy is fragile; about 50% of all pregnancies miscarry, and of these, more than 80% fail within the first three months. http://www.webmd.com/infertility-and-reproduction/guide/pregnancy-miscarriage. For a population under high nutritional stress, where the mother-to-be has insufficient fat to buffer a shortage of as little as 300 calories per day (the cost of maintaining a pregnancy for the first three months), it seems likely that the failure rate could be considerably higher than 50% of all pregnancies. So the woman’s body fat keeps her pregnant.

2. The next thing the woman’s body fat does is get transferred to the foetus. Pond says that for the first half of the pregnancy, the lipids transferred by the mother are used to build the brain and nervous system of the foetus, while in the last three months they go to build the baby’s own fat stores (229). The lipids come off the woman’s thighs and hips.  Let’s tackle these one at a time.

Our big human brain is 60% fat (Pond 24), while the myelin sheathing of our nerves is 70% fat. The retinas of our eyes and – for males – the epididymus are also hogs for fat. www.fi.edu/learn/brain/fats.html. Our intelligence as a species lies in our abnormally large cerebral cortex, which is also 60% fat. Obviously then, it’s really important for our smarts, our vision, and the ability of our men to produce viable sperm and get us pregnant, that mothers should have enough fat in their diets or adipoctyes to deliver a fullterm, healthy child, and then feed it for a protracted period. Pond says, page 229,

“Brain development may be more directly linked to obesity. As pointed out in Chapter 1, the chemical composition of the nervous system has much in common with that of adipose tissue. The brain needs adequate supplies of particular fatty acids throughout its growth period, though once formed, its preferred fuel is glucose. Growth of the foetal brain depends entirely upon essential raw materials extracted from the mother’s blood, which in turn derive from her diet or her adipose tissue.”

Now for the baby fat: first off, human babies are startlingly fat compared with those of other mammals; Pond says merely that “human babies are unusually fat at birth” (229), while Sarah Blaffer Hrdy quantifies it: our infants have 16% adipose tissue at birth, which is 4-8 times as much as other primates (Mother Nature, page 476). It seems to me very likely that baby fat goes to keeping the brain growing; to providing its fatty structure, and not for energy. Why do I think this? Two reasons:

1. Because primates carry their babies, keeping them warm through body contact.

2. Because the brain of human babies is way underdeveloped at birth compared to the brains of other mammals and even other primates; chimpanzee infant brains are about 60% of adult size at birth, while human babies rack up only about 25% of adult size. However, this doubles within the first six months after birth; the only other organ growing at this pace is the eyeball (which also requires astounding amounts of good fat – DHA); the child’s brain has reached adult size by the time s/he is 10 years old (Juhrmain et al, 478). Chimpanzee babies are skinny, and chimpanzee babies don’t have the same brain growth spurt…

Given that human breast milk, like that of other primates, is very low in fat and protein but very high in lactose compared to other animals (Pond 230, Hrdy 476), it seems unlikely that breast milk alone could meet the exploding needs for fat of the mushrooming brain and rapidly growing eyeballs. Lactose is a sugar, highly metabolizable, and an excellent source of energy, which would free up the baby’s fat stores for building rather than burning. Primate mothers nurse very frequently, unlike animals that produce fatty milk, so the infant’s energy requirements are continuously trickle-charged. Further, although breast milk is low in total fat, it contains a seemingly incredible variety of lipids: 199 different fatty acids (Pond 78)!!.

3. Not from Pond; it’s my own idea. Vitamins A, D, E, and K are crucial in the proper functioning of the body, and they are all fat-soluble. It seems intuitive to me that women with plenty of body fat can store lots of fat-soluble vitamins, and transfer them both pre- and post-partum to their babies. Vitamin K is so important to the survival of neonates that it is routinely administered to babies born in developed countries. http://www.livestrong.com/article/372906-vitamin-k-deficiency-in-babies/. Breast milk, being low in fat,  is low in vitamin K, but given the almost constant suckling of babies in premodern societies, this may be sufficient to meet their needs under most conditions.

4. Immunity: breast milk contains factors vital to protecting the baby from infection: http://www.americanpregnancy.org/firstyearoflife/whatsinbreastmilk.html. Obviously, the longer a woman nurses her child, especially during the vulnerable first five years of life, the more likely it is that the child will survive to adulthood and to produce more children. Jack Newman, MD, FRCPC,  in his defense of extended breastfeeding, says “In fact, some immune factors in breastmilk that protect the baby against infection are present in greater amounts in the second year of life than in the first. This is, of course as it should be, since children older than a year are generally exposed to more sources of infection. Breastmilk still contains special growth factors that help the immune system to mature, and which help the brain, gut, and other organs to develop and mature.”
http://www.breastfeedingmums.com/dr_jack_newman_breastfeeding_a_toddler.htm

My point: a lactating woman uses 1000 calories a day to provide milk to her offspring; in times of nutritional hardship, fat stores enable her to continue nursing and supplying these important factors.

This next section is a real kicker: it has to do with sociability, friendliness, and ability to withstand stress! Monkeys fed nutritionally adequate diets high in fat (triacylglycerols and cholesterol), were more sociable than those whose nutritionally adequate diet was low-fat. High-fat-fed monkeys did more grooming, stayed closer together, and better tolerated being moved into new groups – which usually thoroughly upsets them (Pond 227). “The observers concluded that a low-fat diet promoted anti-social behavior, possibly by affecting brain lipids and thereby altering production of the brain messenger molecule, serotonin, the lack of which is known to cause aggression in humans and monkeys” (227-228).

How about this one?

“People with higher blood cholesterol have also been found to be capable of faster mental processing, while those whose levels of cholesterol are unusually low, or have been artificially reduced wth drugs, seem to be more prone to suicide and aggressive behaviour. While there are many possible explanations for these associations, a taste for lipids may have led to a more sociable personality and/or quicker wits, and, as an incidental consequence, to obesity.

These traits may have been valuable for the development of co-operative hunting, ever more complex language and cultural activities such as singing and dancing.” (228).

Or this?

Pond again: “Loss of body fat lowers resistance to disease so effectively that people rarely die of starvation alone unless they are kept away from sources of infection and treated with modern medicines: the immediate cause of death is usually an infectious disease or pneumonia-like infection of the lungs” (232). Among HG San societies, 20% of all babies die in the first year of life, usually from gastrointestinal infections (Shostak 15 ). Could it be that as the babies burn through their birth stores, and their mothers are unable to replenish them because their own diets lack medium and long-chain fats, that they become more susceptible to infection? It would be very interesting to know whether the babies who die are of lower birth weight.

Pond closes her book with this sentence, which I will leave to speak for itself:

“In spite of the much trumpeted health hazards of obesity, we are the longest-lived of all mammals, as well as among the fattest” (314).

Just for fun: Hey Fatty Bum Bum (a lovesong for a large lady)

Hrdy, Sarah Blaffer. 1999. Mother Nature: a history of mothers, infants, and natural selection. Pantheon Books, Random House, Inc., New York, N.Y.

Pond, Caroline. 1998. The Fats of Life. Cambridge University Press, Cambridge, United Kingdom.

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Gelling – or should that be congealing?

Things are coming together nicely now; this is my sequence of thought:

Neandertals and sapiens both occupied the Levant from 130-80kya, during MIS 5a-e, when conditions were warm and moist. Then sapiens vanished, and Neandertals walked alone, like Rudyard Kipling’s cat, through 25,000 years, from 75-50kya. Then Neandertals disappeared from the record and from the Levant, while sapiens moved in and has occupied the region ever since. We know that Neandertals were cold-adapted, which would have given them an edge during MIS 4, when the Levant was cold and dry – BUT we also know that they did very nicely, thank you, during the previous warm wet phase of 50,000 years, so it’s hard to see why the return of better climatic conditions would shove them off the cliff.

Something had changed for Anatomically Modern Humans; it has been argued that the development of projectile weaponry widened the range of prey available to sapiens and that provided them with more food. However, this seems unlikely, as Leslie C. Aiello & Jonathan C.K. Wells  argue that humans can metabolize only enough meat to meet half of their energy requirements; digesting and assimilating meat uses a lot of energy, which is why modern paleo dieters eat so much fat. Further, eating a lot of meat sharply depresses one’s appetite (2002: 326-327). This could be a serious problem for a pregnant or lactating woman. Dietary fat is a good energy source, but it was in short supply during the Palaeolithic; game animals tend to be very lean for much of the year, say John D. Speth & Katherine A. Spielmann (1983: 3-5), and vegetable oils were firmly locked into vegetable parts (like pistachios) instead of glistening gold in bottles under supermarket lights. It would also likely be difficult for women to gorge on meat, even when hunting was good; historically, the ownership of meat in hunter-gatherer societies was vested in the hunter, who doled out his kill according to social norms; the San woman, Nisa, as recorded in Marjorie Shostak’s ethnography of that name, divorced her second husband for refusing meat to her father. Nisa’s father, who engineered both the marriage and the divorce, wasn’t bent out of shape by her husband’s refusal of meat to Nisa, but immediately decreed an annulment when the hunter wouldn’t give him any (1983:140-142).

Brown and Konner  state that humans, not even obese humans but just people with a normal amount of body fat, are among the fattest of all mammals (2006:30). Unlike other mammals, however, we don’t use our fat as insulation against cold – it’s our energy  storage organ, like a camel’s hump. And across cultures, even among very lean people like the San, women carry almost twice as much fat as men despite being very similar in height and weight. For primate females, says Sarah Blaffer Hrdy in “The Woman That Never Evolved,” there is one main goal: the most efficient conversion possible of resources into offspring (93). Is some unfortunate dead horse being flogged here?

Getting to the point: it is apparently extremely important for women to have a fair amount of fat, and this need is driven by the species’ need to reproduce.

Some questions:

1. How do we get fat? Gary Taubes insists that fat is laid down from the eating of carbohydrates.

2. Were women fat before the revolution that wasn’t? Let’s look at art before the 80kya point at which sapiens were seen no more in the Levant, and after the 50kya point at which they resurged.

3. Where could women lay their hands on surplus carbohydrate? Is there any suggestion or -better yet – evidence that carb-rich foods like berries, other fruits, and tubers, are regarded as women’s food, and low status, in HG societies?

I’ll be back. As Swami Beyondanda says, I will answer the questions, and you will question my answers!

Aiello, Leslie C. and Jonathan C.K. Wells. 2002. Energetics and the Evolution of the Genus Homo. Annual Review Anthropology. 31:323-38.

Brown, Peter J. and Melvin Konner. An anthropological perspective on obesity. 2006. Annals of the New York Academy of Sciences 499: 29-46..

Hrdy, Sarah Blaffer. 1983. The Woman That Never Evolved. Harvard University Press, Cambridge, MA.

Shostak, Marjorie. 1981. Nisa. Random House, Inc. New York, NY. Chapter 8: First Birth. Chapter 9: Motherhood and Loss.

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