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Domestication Due to the Neural Crest

"Domestic fox"

“Domestic fox”

The latest issue of Genetics has an interesting hypothesis paper, The “Domestication Syndrome” in Mammals: A Unified Explanation Based on Neural Crest Cell Behavior and Genetics. It sounds grand, but if you read the details it makes a lot of sense that changing the developmental pathway of neural crest cells has perturbed a great many traits. The target of selection in this case is “tameness,” the exact parameters of which they elucidate in the text. But there are numerous other phenotypic side effects which are hallmarks of domestication. Basically these are likely the outcome of the genetic correlation, as a given genetic alteration can have multiple downstream consequences. The paper is open access, so I invite you to read it yourself and make up your own mind.

For me the most interesting point is the argument that across mammals (and perhaps other vertebrates!) the disruption of development is due singularly to changes in neural crest cells, but on the genetic level the evolutionary process is polygenic and diverse. In other words the developmental pathway will exhibit similarities, ergo, similar correlated side effect traits. But the genetic architecture of the change across species may vary, because there are many genes which are effected by the phenotypic target of selection. Another way to state this is that there is no gene for domestication in the lineages under consideration, but rather many genes which have significant, but not overwhelming, effect. Of course there’s polygenic, and then there’s polygenic. One of the common side effects of domestication is depigmentation of the pelage of mammals, but this is one case where the number of genes effecting the trait is relatively low, on the order of ten genes account for more than half the variation. In contrast you have polygenic traits like height where you’re lucky to find one locus which can explain one percent of the variation. If domestication is like the latter then the role of standing variation in the evolutionary story is going to be large, nearly total. In contrast if pigmentation is representative than classical selection on new mutations of large effect unique to particular lineages may still be important. Not to be lame, but the answer is probably going to be in the middle, on average.

Second, there are broader questions about contingency, the genetic architecture of salient traits, and selection as a driver for adaptation, which come to mind after reading this paper. It seems hard to deny that if you constrain the phylogenetic space enough then there are many instances where evolutionary forces will basically result in broadly similar phenotypic and genetic outcomes. Though there are some differences in traits and genetic variations, there is a great deal of overlap across mammalian taxa which have been targeted by artificial selection. Though the authors don’t address this directly it, seems clear that many of the phenomena which revolve around domestication also apply to humans. If they do, and if “domestication” occurs through gradual selection upon standing variation, then the search for the gene which makes us uniquely human (e.g., “the language gene”) may be futile. Rather than a gene, our humanity may have emerged out of gradual change as the underlying frequency of alleles is shifted. This is not a sexy answer which will result in genomic fame for a researcher who discovers the gene-which-makes-us-human. Finally, there is the issue where we bracket artificial selection and domestication as if they are unique processes which derive from human agency. My own position is that though for semantic purposes we may speak of ‘artificial selection’,’ sexual selection’, and ‘natural selection,’ there’s really no fundamental difference at the root for these phenomena. Selection is selection, and the rest is commentary. To me that implies that attempting to understanding domestication may actually allow us to understand evolution more broadly (and Charles Darwin would agree with that point I suspect).

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  1. B&B
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    Artificial selection grades into natural selection because of commensals and landraces. Though humans ourselves, our commensals and our livestock have all been subject to comparable evolutionary pressures in the Holocene there is no consistency in the zootaxonomy. St Kilda house mice are granted full subspecies status despite their quite minimal difference from other house mice. Normally domestic animal livestock are not divided into subspecies except to recognise historically separate domestication events (cattle) but exceptions are maintained for long-term feral stocks such as the southwest Pacific pariah dogs, wild goats of Crete and Europe’s moufflon.

    Luckily biocultural evolution makes these two concepts redundant nowadays, but there is still the taxonomic mess left to sort out. If taxonomy is to be consistent then how many subspecies of man are extant, and on what grounds ought they to be recognised? Landrace is ecotype but evolutionarily significant clusters of ecotypes can nonetheless be recognised using standard morphological criteria.

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  2. Hepp
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    ‘then the search for the gene which makes us uniquely human (e.g., “the language gene”) may be futile.’

    Isn’t FOXP2 something like a “language gene”? If not, what would a language gene look like?

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  3. Razib Khan
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    foxp2 is important. but it isn’t both necessary and sufficient.

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  4. You know, I do not really think that humans, despite displaying some of the characteristics of “domestication” – such as reduced snout and body size, reflect the same pattern of selection.

    The fact that humans have generated a niche, – an anthro-ecology – to which other mammals have become adapted through natural and “artificial” selection, is clear. And I agree with you, Razib, that it it is quite true that humans, being part of nature, constitute agents of natural selection along with other species like wolves and ants which also alter the selection pressures on their prey and/or symbiotes. So, following your thought here, the term “artificial” for human-associated selection pressures is special pleading… and, of course, even Darwin recognized this.

    Can we really make the case for humans being an examples of domesticated animals, however? I am not persuaded. Can we really think that there has been analogous -or homologous – domestication in humans during any recent period of our species history? Are contemporary hunter-gatherers more aggressive than the residents of London or New York? Is the “egalitarian syndrome” the opposite of the “domestication syndrome”?

    I think this is a fair question.

    In almost every case, alterations to polymorphisms effecting neural crest have occurred due to specific changes in levels of adrenal response. The triggering of the fear and fight/flight in response to human presence happens at much higher levels of stimulation in domestic dogs vs tamed wolves. The aggressive dominance behaviour normal for wild wolves is also constrained, — although Chihuahuas may be an exception, haha– and there is also evidence, discussed in the paper by Wilkins et al that you have cited here, at least in dogs, of a prolonged and more generalized imprinting period, permitting puppies to imprint on humans if handled even for short periods of time before the age of three to seven months, which is three to five times longer than in wolf puppies.

    There is a lot of past research already being put to practical use here, especially in horses and other large mammals that need to be handled at some point during their adult lives. So the lengthening of the imprinting period is of vital importance in understanding domestication. It also, of course, has long been employed in the training of sheep guard dogs, and other flock guardians, and appears to redirect aggression in breeds that guard humans, such as wolfhounds and other sighthounds, as part of a dual utility (as the sighthounds were also expected to be hunters). I was fascinated that the prolongation of this imprinting period is actually related to the other aspects of domestication via the neural crest-related down-regulaiton of adrenaline. For further examples of imprinting see the material here: http://animalbehaviour.net/Imprinting.htm

    Recent research into the genetics of behaviour, especially aggressive behaviour, in dogs indicates that there are many different genes involved, with polymorphisms affecting several different neurotransmitters either through altering their production (repeater variance affecting dopamine do exist in dogs as well as in humans and most other mammals: and I quote:

    “…dopamine D4 receptor, the long form of which is associated with risk seeking behavior in humans (Noble et al. 1998) and monoamoine oxidase A, an enzyme which breaks down dopamine and a mutation of which is associated with incarceration of humans, if they had a bad childhood environment (Caspi et al. 2002)…”
    However, a paragraph further on in the paper cited above on dog behaviour, the authors say:
    “…The results of the candidate gene approach to canine aggression have been uniformly disappointing so far. Although Nimi and colleagues (1999) showed that a usually gentle breed of dog, the golden retriever, had the short form of the dopamine D4 receptor and the territorially aggressive Shiba has the long form, this is not associated with behavior but rather with the genetic differences between an Asian and an Anglo-American breed (Parker et al. 2006).” source: http://actavet.vfu.cz/pdf/200776030431.pdf

    Cattle show genetic signatures of domestication similar to that in dogs:

    “…Domestication of cattle provides an excellent model of animal evolution. During the domestication process, cattle have adapted in morphology, physiology and behavior to captive life… The phenotypes associated with domestication include milk and meat production, fertility, appearance including coat coloration, decreased fearfulness, social motivation, and mild temper [6]…..” (source: http://www.plosgenetics.org/article/info%3Adoi%2F10.1371%2Fjournal.pgen.1004148 )

    More recent research on domesticated cattle has revealed that there was likely to have been a third centre of Taurine domestication in Africa. As with dogs, it impossible that different genes for aggressive behaviour were targeting by humans during domestication, accounting for the complex differences in this kind of behaviour , especially in bulls. http://www.plosgenetics.org/article/info%3Adoi%2F10.1371%2Fjournal.pgen.1004254

    Down-regulartion of the adrenal response, due to its complex links with neural crest deficiencies, is not altogether benign. Selection for tameness in white tailed deer has become associated with both albinism and pie-bald colouring, and these are furthermore linked to defects of metabolism, hearing, and joint problems. As long ago as 1980, there were cautions that use of hypo pigmented (albino) animals in research was not to be recommended due to the other abnormalities associated with it – this could be related to abnormal neural crest development as well ( http://www.sciencedirect.com/science/article/pii/009130578090461X).

    As an aside, I might mention that in the domestication of fermenting yeast the domestication process was primarily metabolic: http://www.sciencedirect.com/science/article/pii/S0960982212005866

    However, back to humans… I find the suggestion by Wilkins et. al. that there might be “epi-mutations” involved, due to cross generational epigenetic effects (especially lower stress levels) rather farfetched. We do not after all, know what the rate of conception vs fetal loss is, and this might be altered by levels of maternal stress, and could result in prenatal selection favouring certain pre-existing mutations over the wild type – and this might account for the higher than expected incidence of variants such as the “Star” mutation.

    However, what if we explore, not human “domestication” as the opposite of egalitarianism, but as it’s cause, we set back the timing of this hypothetical process by some 3 million years. Assume that our common ancestor with Pan troglodytes and Pan paniscus was more aggressive in social interactions, and had groups typically incorporating a dominance hierarchy which affected reproductive success.

    I don’t think I am suggesting we are going out on any precarious limbs here.

    These animals were undoubtedly using branches and rocks and bones as tools… and possibly as weapons. Further, assume that this dominance hierarchy, and particularly the kind of aggressive behaviour towards subordinates, thus became too dangerous to be tolerated. A cuff or bite is one thing, but getting hit with a big rock or tree branch is something else entirely.

    What if we assume that severely aggressive behaviour was systematically disabled by groups of subordinate individuals ganging up and either killing or marginalizing the most aggressive males (as Christopher Boehm has suggested in “Moral Origins” and elsewhere? Furthermore, assume that this process, over the course of fairly short periods of time, resulted in a positive selection for cooperative and “tame” behaviour among members of social groups. this wold reduce the need for big canines, and result in shorter snouts. Behavioural shifts would result in less stressful social inter-actions, and more access to food for young and therefore subordinate animals. Movement of individual, males and females, among groups would be less difficult if it no longer meant aggressively working one’s way up a dominance hierarchy.

    This leads us to another twist in the selection process, of course. For you cannot get a bunch of wimps to take on the big bully, even if they have numbers on their side. If cooperative action against a dangerous aggressive male is to result in ouster or assassination, rather than him beating you and all your buddies up in retaliation, you can’t afford to be TOO tame. You still need that mobilizing capacity for outrage, and considerable capacity for courage and steadfastness. School children routinely practice all these moves, although at times bullies manage to form gangs of their own followers, and the mayhem, without adult supervision, can be truly awful.

    What this means is possibly that the domestication syndrome had to shift gears at some point and become the egalitarian syndrome. High courage became attached to the protection of the young and the weaker (women, children and younger and well as elderly males) from the strong (big dominant males). furthermore, collective preventative action was the most likely to succeed. There may be a very good reason humans almost universally root for the under-dog and tell stories of how youngsters -especially boys – learned to become men by taking on a scary opponent with the help of friends. Today we have to wonder if we humans can afford to be domesticated, for it is this same courage in the face of injustice that brings out crowds at protests, that speaks truth to power, and fights for freedom and democracy all over the world.

    If the population was small and very scattered, the role of mate preferences, based on sensed heterogeneity, especially the Major Histocompatibility Complex, could be more easily accommodated by freer movement of personnel between groups over a wide area. Tolerance, by males, of female mating preferences might have led to lengthening consort-ships, mutual provisioning, and co-parenting between couples. More involvement in care of the young appears to be linked to reduced testosterone in modern humans; might this have contributed to lessening of hormone-fueled hostility among males? Shortening of the snout, and reduced body size might have made sense in an animal adapting to a marginal habitat on the forest edges, especially if food sharing was facilitated by less aggression.

    Once this degree of “domestication/egalitarianism” was achieved, the stage would be set for changed entrained by control of fire. Using it for food processing and protection permitted them to sleep wherever they made camp, and to use the safety and convenience of its heat and light, to form a sharing place, where several couples and their young could rest and play on the ground. And Richard Wrangham’s hypothesized reduction of teeth and jaws, “the cooking hypothesis” might explain just what other selection factor kicked in at this point, at the dawning of the genus Homo.

    After thought:
    I might also add that research into the effects of alcohol on developing mammalian fetuses results in abnormalities also traceable to neural crest: http://onesci.com/journals/science_journal_20.pdf As do the effects of the toxin in Corn lilies (cyclopamine) and a number of other toxins. This means that during domestication, interference with neural crest development is often constrained by increasing levels of debilitation and lethality (see also: http://dev.biologists.org/content/125/5/813.full.pdf )

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  5. Razib Khan
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    helga,

    thanks for the long comment. lots to think about. re: However, what if we explore, not human “domestication” as the opposite of egalitarianism, but as it’s cause, we set back the timing of this hypothetical process by some 3 million years.

    yes. i’m thinking less recent human evolution, and more the emergence of sapiens as we understand it. though i think there are likely some differences between modern groups too. if a lot of this is due to selection on standing variation then the distribution is likely to be somewhat different between different mating groups in different ecologies (ecology being the human social environment).

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  6. B&B
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    Helga, you ask if we can we really think that there has been analogous domestication in humans during any recent period of our species history.

    The answer is yes, since the end of the Pleistocene humans have gracilised and our brains have gotten smaller in line with the other domesticated mammals. Like the Winegards pointed out, expecting a ‘universal mind of man’ over the inference that how cognition and behaviour has changed thanks to genes, is a kind of dualism (and the special pleading fallacy as well.) Although few if any genes have been identified demonstrating a biological basis for the differences between populations, their existence is soundly predicted.

    A consequence of this might be that (non-intensive) hunters and foragers would be inassimilable to settled life, and that hybrids would have reduced reproductive success in a Neolithicised society. It is actually suggested in the research literature that ADHD traits reflect normal hunter-forager personality traits sporadically emerging in a setting where such individuals appear disordered.

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  7. Razib Khan
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    if this is operating through *standing variation* then we need to start qualifying the talk in terms of “types” (e.g., HG vs. farmer). seems like you’ll see distribution differences. disjoint? unlikely. but if 10,000 years of dense living have reshaped the immune systems of long term farming pops, i see no reason why we shouldn’t expect changes in personality, etc. just needs to be founded in fact rather than spec in terms of details.

    A consequence of this might be that (non-intensive) hunters and foragers would be inassimilable to settled life, and that hybrids would have reduced reproductive success in a Neolithicised society.

    in terms of quantities, i think the non-categorical aspect is important to point out. looks like southeast asians are 25% or so non-northeast asian. that is, non-farmer. initial pop mixing might have been higher fraction of austro-melanesian element, but selection reduced overall frequency. but this is selection on extant variation across distributions, so the stark assertions you see in bellwood’s *first farmers* probably not tenable.

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  8. B&B
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    Vegeculture was likely practiced in much of SEA before the arrival of Mongoloid peoples, and life largely more settled than if we imagine the whole region inhabited by some kind of full sized proto-Negritos following strictly LPA subsistence patterns. Phytoliths demonstrate the early presence of a New Guinean domesticate as far away as the Philippines at a very early date of >8kbp (Dioscorea alata at Ille Cave, Palawan) and a suite of cultural traits broadly connected to an ‘arc of vegeculture’ also round into Nepal.

    The 25% non-NEA ancestry of SEAs today is likely then from people with a subsistence pattern comparable to the precolonial Melanesians, with food production mixed together with the exploitation of wild resources.

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  9. Um no, B&B, that process of reduction of body size and finer bone started long before Holocene, it has been ongoing in most populations (all of them foragers) since at least 40,000 years ago. It began during the last Ice age, when spear throwers and other distance hunting technologies were invented, like bows and arrows and blowguns and boomerangs. in southern Africa these have been dated to at least 60,000 years ago.

    These made hunting safer, and seems to have replaced emphasis on size and strength with more emphasis on stamina and skill. Once that happened, it made smaller and lighter people more calorically economical. Not only did you not have to wrestle with large game animals to bring home meat, but you could afford to have smaller women who could produce large brained babies using fewer calories.

    The other flaw in your model is the assumption that almost all humans switched to farming in the Holocene. In fact only a tiny percentage did it, probably in fits and starts for thousands of years, beginning in particular environments, around the world. Even three thousand years ago, nearly half the world’s population was pursuing a foraging economy.

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  10. B&B
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    It doesn’t matter exactly when it began, if its been an ongoing process into the Holocene. To this day robust ecotypes correspond to the uplands of a region like Iberia or Wales with gracilisation (domestication) corresponding with urbanisation. If you compare a cross-continental modern human sample with one of UP Homo sapiens we’re gracilised.

    In any case the importance of hunting in the Upper Palaeolithic is overestimated down to the preservation bias favouring lithics over the techniques used by hand collectors. Hence ecological analogues of Fuegian guanaco hunters can be assumed to have left most trace fossils even though ecologically the peoples of the time must’ve been diverse like the ethnohistorical LPA communities. Things like baskets and even passive snares simply aren’t preserved with anything like the same frequency. I don’t understand why people push the importance of large game hunting in the evolution of Homo, knowing hand collecting to be the plesiomorphic state shared with apes, which means shifts to specialised predation are repeated divergences from the norm.

    Clearly Mesolithic Europeans were more gracile than the Palaeolithic big game hunters whose limb proportions resembled those of the ecologically similar Fuegians. And TBH this seems a concrete demonstration of domestication through sedentism, since Mesolithic western Europeans were more sedentary than their predecessors. (Sedentism obviously does not depend upon food production where available resources facilitate intensified exploitation by larger communities.)

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  11. http://www.pasthorizonspr.com/index.php/archives/07/2014/70000-year-old-african-settlement-unearthed

    70,000 YEAR-OLD AFRICAN SETTLEMENT UNEARTHED
    Article created on Sunday, July 20, 2014

    During ongoing excavations in northern Sudan, Polish archaeologists from the Institute of Archaeology and Ethnology in Poznań, have discovered the remains of a settlement estimated to 70,000 years old. This find, according to the researchers, seems to contradict the previously held belief that the construction of permanent structures was associated with the so-called Great Exodus from Africa and occupation of the colder regions of Europe and Asia.

    The site known as Affad 23, is currently the only one recorded in the Nile Valley which shows that early Homo sapiens built sizeable permanent structures, and had adapted well to the wetland environment.
    This new evidence points to a much more advanced level of human development and adaptation in Africa during the Middle Palaeolithic.

    Locating the “village”

    “Discoveries in Affad are unique for the Middle Palaeolithic. Last season, we came across a few traces of light wooden structures. However, during the current research we were able to precisely locate the village and identify additional utility areas: a large flint workshop, and a space for cutting hunted animal carcasses, located at a distance” – explained project director Dr. Marta Osypińska.
    The researchers are also working on a list of animal species that these early humans hunted. Despite the relatively simple flint tools produced using the Levallois technique, these humans were able to hunt both large, dangerous mammals such as hippos, elephants and buffalo, as well as small, nimble monkeys and cane rats (large rodents that inhabited the wetlands).

    Palaeolithic hunters

    This year, the researchers intended to precisely date the time period in which the Palaeolithic hunters lived here, using optically stimulated luminescence.

    “At this stage we know that the Middle Palaeolithic settlement episode in Affad occurred at the end of the wet period, as indicated by environmental data, including the list of hunted animal species. But in the distant past of the land such ecological conditions occurred at least twice” about 75 millennia and about 25 millennia ago. Determining the time when people inhabited the river bank near today’s Affad is the most important objective of our project “- said prehistory expert Piotr Osypiński.

    The Polish team is working with scientists from Oxford Brookes University, who are helping to analyse the geological history of the area. The results will help determine climatic and environmental conditions that prevailed in the Central Nile Valley during the late Pleistocene and hope to identify factors that contributed to the excellent state of preservation at the Affad 23 site.

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  12. And yes, it does matter. All African hunter-gatherers are “gracile”, so are the Australian Aboriginal peoples and the Inuit… for example. So give it up, my friend.

    The fact that people got even shorter, after they began to live in sedentary communities in the post-Neolithic, and even Mesolithic period, is a consequence of increased rates of malnutrition and disease. In industrial populations, we begin to see partial recovery to pre-Neolithic heights but this is well understood as secular trend, and it occurs due to less infectious disease, lower parasite load, and adequate, even excessive, dietary changes. I say excessive because processed foods, leading to high sugar and starch consumption, particularly in infancy, appears to force a maximization of body fat (target organ size), overall height and weight, and reduced age of puberty, (although, not, sadly of faster maturation of the prefrontal cortex) sub-optimal in terms of human health, let alone life history.

    I can supply lots of links to research showing all this, but I don’t suppose it would make any difference to an entrenched opinion. If not so entrenched as you appear, if you want to learn about this, just say so.

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  13. Razib, you seem to have a rather extravagant notion of the number of humans who could be said to being living at high densities in the year 10,000 BP, or even in the year 5000 BP.

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  14. B&B
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    I have already explained that gracility is relative, it doesn’t change that we are gracile compared to the UP ancestral people. Lieberman demonstrated this global trend in one of his papers. And whether the trend of self-domestication actually began prior to the Holocene is irrelevant since it must, logically, have proceeded in the different regions at different rates. I don’t think anyone doubts that AMH appear domesticated relative to other hominins, but what matterd is this doesn’t entail that process became stalled back in some EEA. And no one is suggesting sedentism or urbanisation are responsible for the gracility of people like interior Australians.

    There are obviously other effects causing gracility besides sedentism. Desert populations and short statured rainforest populations are obviously gracile but its obviously for a different reason. ‘Murrayans’ are more robust than the classic desert Aborigines, likewise its no surprise that Kalahari people in Africa are not as robust as their ‘full sized Bushman’ ancestors, the old South Africans having been pushed into less hospitable areas. Pygmies are also gracile in harsh rainforest environments that might be compared nutritionally to deserts since the edibles are mostly up out of sight. But today’s hunter foragers are largely unrepresentative of Pleistocene people and follow their own evolutionary pathways, both culturally and phenotypically.

    Since most of us don’t live in deserts and we aren’t rainforest pygmies, so our tendencies towards gracility needs another explanation than theirs and no truly global explanation for this trend can possibly exist and in places like Terra del Fuego there remained exceptions to the overall trend – because neither sedentism nor living in deserts or rainforests ever applied to them. In our case as sedentary Europeans our gracility – and correlating traits – have to relate to our own evolutionary history not that of other populations. Also sedentism itself does not merely decrease robusticity it has other effects as well ie. the cranial index, its certainly not just people’s height or robusticity of the skeleton that has changed.

    Furthermore I’d also question the statement that health trends were straightforwardly declining since the late UP till the modern period, despite the variety of ecological situations prehistoric humans must’ve found themselves in, and the diversity of techniques that must’ve been in existence to obtain or process food, or to deal with parasitic diseases. Surely the statement has to rest on a possibly nonrerpresentative sampling for any given period of time.

    If we’re going to get a bit rude over who has ‘entrenched opinions’ it seems you think the rest of us are unaware nutrition affects height, we already know everything in the next to last paragraph. ~_^

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  15. Account for this then: http://www.randalolson.com/2014/06/23/why-the-dutch-are-so-tall/

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  16. Nibbles: BBC series, Pacific breadfruit & yams, Sustainable diets, Cuba atlas, MSB standards, Biofortification on radio, German food scandals, Mexican foods, Non-PC food, CWR interviews, Old Irish sources, ITPGRFA funding, Crop Trust presentations, IS
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    […] A theory of mammal domestication. […]

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  17. B&B
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    But I have not denied that diet affects height. That would be silly as denying heredity affects height.
    And indeed Dutch (ie. ‘Nordic’) morphotype is inherently tall and slender limbed like the UP Europeans. I don’t know why this is when the Dutch are settled, and such proportions are in temperate populations connected to big game hunting and impair conservation of heat, but they are not the only exceptions to such rules (Polynesians famously have a cold climate somatype in the tropics.)

    Indeed the Edit (6/29/2014) itself mentions Dutch genes so I don’t see what your point is.

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