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paleoanthropology, genetics and evolution

migration

  • Taking the mtDNA pulse of Neandertal populations

    Tue, 2012-02-28 11:01 -- John Hawks

    Neandertals have strikingly limited genetic variation. They once lived across a range from Spain to Siberia. Yet when we compare sequences across their whole genomes, we find them to be much less different across this geographic range than people living in the same regions today.

    I think this is one of the most fascinating findings of ancient genomics. It may tell us something about Neandertal populations that we did not begin to suspect without their DNA.

    But there is one explanation for this fact that I and others pointed out long before DNA evidence: The Neandertal population was surely much, much smaller than Holocene population of Europe. Small population size over a long time can restrict genetic diversity. So maybe the Neandertals preserved little genetic variation simply because there were so few of them.

    Neandertal mtDNA dynamism

    Love Dalén and colleagues [1] add some perspective to this question. The paper adds one novel mtDNA sequence, of the Neandertal from Valdegoba, Spain, to the record of Neandertals. This builds on earlier work by Ludovic Orlando and colleagues, who performed some analysis of Neandertal variation over time when they reported the sequence of the 100,000-year-old Scladina mtDNA sequence [2]. The main contribution of the current paper is its separation of Neandertals into earlier and later subsamples, showing that the Neandertals after 48,000 years ago in Western Europe have greatly restricted mtDNA diversity compared to the earlier sample of Neandertals.

    That's a tricky comparison. The paper illustrates it with this figure:

    Neandertal mtDNA phylogeny from Dalen et al. 2012

    Figure 1 from Dalén et al. 2012. Original caption: "Figure 1. Phylogenetic relationships and geographic distribution of Neandertals. Recent (<48 kyr) western Neandertals are placed within a well defined monophyletic group (blue box), whereas specimens older than 48 kyr constitute a paraphyletic group together with eastern Neandertals (red box). The sampling locations for the specimens are shown with corresponding colour coding."

    The blue clade includes all Neandertals after 48,000 years ago from Western Europe; the red clade includes earlier Neandertals from the west as well as both earlier and later Neandertals from the east.

    The meat in this phylogram is not only that the later western Neandertals are close relatives, but that they share an ancestor only around 60,000 years ago. That's a mere 20,000 to 25,000 years before the later western Neandertals lived. The variation within these Neandertals is roughly the same as that within a single mtDNA clade within Europe today, such as clade H1.

    Comparing the later Neandertal diversity to the variation of present-day Europeans helps to clarify the meaning of low diversity. Low mtDNA diversity doesn't necessarily imply that the later Neandertals in western Europe were few in number. Certainly there are millions of Europeans today who carry clade H1, for example. Low mtDNA diversity tells us something more limited about the ancestors of these Neandertals. Sometime after 60,000 years ago, a pulse of mitochondria came from the east and were remarkably successful in the west.

    Looking at the red clade in the figure is also illustrative. Eastern Neandertals and earlier western Neandertals had a lot more diversity than the later western Neandertals. We have to remember that the Scladina individual lived 40,000 years before the common ancestor of the blue clade, so that the greater ages of these specimens matters. Still, when we look at the diversity in that red clade, it is greater than the mtDNA diversity today in the most widespread basal clade outside Africa, the M clade. Taking the mtDNA phylogeny alone, we would say that the 13 Neandertals had a greater sequence difference than all the people who with ancestry outside Africa today. Only when we look at the predominantly African clades today (the L clades) do we start to see sequence differences as great as among these Neandertals.

    I began the post by pointing out that small population size alone might explain the low mtDNA diversity of Neandertals. Dalén and colleagues provide a key comparison that helps to reject that hypothesis. Small population size alone cannot explain the discrepancy of mtDNA diversity of these Neandertals across space and time.

    The whole-genome perspective

    Now, the question is whether this pattern holds true only for mtDNA, or whether the rest of the genome also shows some dynamic within Neandertal populations.

    We have quite a lot of information on this point, because the initial sequencing of the Vindija Neandertals was accompanied by a smattering of sequencing of the nuclear genomes of one individual from El Sidrón, the original Feldhofer specimen and the Mezmaiskaya Neandertal specimen. The inclusion of Mezmaiskaya is important, because it alone is not included in the "low mtDNA diversity" red clade pictured above. If the pattern observed for mtDNA is reflected by the rest of the genome, the comparison between Mezmaiskaya and western Neandertal genomes should show substantially more diversity.

    When they published the draft Denisova genome, Reich and colleagues [3] used it as an outgroup to investigate variation among the Neandertals, and they focused initially on Mezmaiskaya:

    Using the 56 Mb of autosomal DNA sequences determined from [the Mezmaiskaya specimen], we estimate that the DNA sequence divergence between the Vindija and Mezmaiskaya Neanderthals corresponds to a date of 140,000 +/- 33,000 years ago (Supplementary Information section 6) (Fig. 1). This remarkably low divergence—which is about one-third of the closest pair of present-day humans that we analysed—is in agreement with the observation that diversity among Neanderthal mtDNAs is low relative to present-day humans and indicates that the Vindija and Mezmaiskaya Neanderthals descend from a common ancestral population that experienced a drastic bottleneck since separating from the ancestors of the Denisova individual.

    That adds substantially to the mtDNA picture. The mtDNA variation of western Neandertals may reflect population turnover after 50,000 years ago. But the nuclear genome comparison cannot be explained by this single event. The variation of nuclear genomes between Mezmaiskaya and El Sidrón spans across more than half the Neandertal geographic range and requires mechanisms that restricted genetic variation across at least the period after 140,000 years ago.

    I think we can do quite a bit better using the nuclear genetic information already available, keeping an explicit phylogeographic model in mind. My view is that Neandertal populations were dynamic throughout their existence, with repeated waves of population turnover across broad geographic scales. The mtDNA of later western Neandertals may reflect a large, recent event. But there must also have been earlier ones to limit variation of the nuclear genome. The implication is that early Neandertals like Krapina may have had relatively little genetic connection to later Neandertals in the same region, like Vindija.

    That picture matches what we are beginning to understand about the population history of Europe during the last 30,000 years. I think that's how human populations have always behaved.

    Revisiting Neandertal races

    I wrote extensively about Neandertal mtDNA in 2009, noting the work of Virginie Fabre and colleagues [4], which showed the geographic structure of Neandertal mtDNA variation ("Neandertal races?"). Fabre and colleagues showed that Neandertal mtDNA variation is apportioned unequally across space, and made sense of the variation using a phylogeographic model with three broad geographic groups. I pointed out then that an alternative explanation might be that the specimens represent different times:

    Many have pointed out, going back to McCown and Keith (1939), that time is another possible cause of morphological differentiation of Neandertals. The mtDNA sequences cover a wide range of times -- the Scladina sequence comes from roughly 100,000 years ago, the others cover the span from 50,000 down to 29,000 years ago. Why not test temporal groups instead of geographic groups? Temporal clusters might reflect interglacial colonizations, differential gene flow, or natural selection. There is a good precedent -- last year a report of complete mtDNA sequences from woolly mammoths found evidence for geographic structure among mtDNA lineages, one of which apparently replaced the other (Gilbert et al. 2008).

    Time is just one example of an alternative model for variation. But I think it helps to clarify the basic problem of the a priori models -- you have to draw boundaries between the specimens somewhere.

    The problem still remains even in the current paper. Why should we divide time arbitrarily at 48,000 years ago? Why divide time in western Europe but not across the eastern part of the Neandertals' range?

    Combining space and time into a single phylogeographic picture is complicated. We end up using a null model to generate millions of pseudosamples to represent the exact time and place we found specimens, hoping to show the null model wrong. Refuting a null model doesn't necessarily tell us much about the behavior of ancient populations that flowed across space and interacted at different times. I think that life was more complicated rather than less, and look to models from more recent populations to understand it.

    How not to publicize your work

    The paper by Dalén and colleagues is such a neat piece of work, I think it's a shame that Uppsala University had to go and spoil it with this silly press release: "European Neanderthals Were On the Verge of Extinction Even Before the Arrival of Modern Humans".

    The paper pointedly does not show that Neandertals were on the "verge of extinction". Neandertals in the eastern part of their range show no sign of any demographic collapse, and the western part of the range arguably only shows signs of recovery and expansion.

    What the paper actually tells us is about the dynamism of Neandertal populations, which is very comparable to that of the Europeans of the last 10,000 years. Keeping this comparison in mind helps remind us that very large groups of people may still have low mtDNA diversity, reflecting the history of population movements and interactions in the past. Comparing the mtDNA with nuclear genetic evidence is also essential to this picture. Neither of these tell us that Neandertals were near extinction.

    Please, if you're putting together a press package about Neandertals, stop framing it around the concept of Neandertal extinction. You aren't going to say anything novel about this, and it just encourages lazy science writing. And it's a false concept. The Neandertals didn't become extinct.

    UPDATE (2012-03-06): A reader points out that several of the dates for specimens in the paper are different than reported in the literature. I noticed that too, and don't know quite what to make of it. I don't think that the differences in dates affect the general result, that later specimens in Western and Central Europe are relatively invariant compared to the Eastern European and Asian sample. But it is a reminder that the results do depend on a certain ordering and geographic sampling of specimens and may change if we fill in the gaps.

    References

    1. Dalén L, Orlando L, Shapiro B, Durling MB, Quam R, Gilbert TMP, Díez Fernández-Lomana CJ, Willerslev E, Arsuaga JL, Götherström A. Partial genetic turnover in Neandertals: continuity in the east and population replacement in the west. Molecular biology and evolution. 2012;29(8):1893-1897.
    2. Orlando L, Darlu P, Toussaint M, Bonjean D, Otte M, Hänna C. Revisiting Neandertal Diversity with a 100,000 Year Old mtDNA Sequence. Current Biology [Internet]. 2006;16:R400–R402. Available from: http://dx.doi.org/10.1016/j.cub.2006.05.019
    3. Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PLF, et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature [Internet]. 2010;468:1053–1060. Available from: http://dx.doi.org/10.1038/nature09710
    4. Fabre V, Condemi S, Degioanni A. Genetic evidence of geographical groups among Neanderthals. PloS one. 2009;4(4):e5151.
    Tags: 
    Neandertal DNA
    mtDNA
    Neandertals
    population dynamics
    migration
    phylogeography
    Synopsis: 
    Neandertals in western Europe have a recent mtDNA ancestor, pointing to the dynamics within their population.

  • Mailbag: Neandertal genes across the Strait of Gibraltar

    Sun, 2012-02-12 22:03 -- John Hawks

    Re: Neandertal gene variants in Yoruba:

    If you think in terms of ice-age climate, with sea-level about 150 ft lower than at present and the Mediterranean regularly covered by thick arctic-like ice in winter, it is easy to imagine early humans making their way back and forth over an ice-covered strait of Gibraltar or along an ice-free coastal strip connecting western Europe with West Africa. I think the discovery of relatively large number of neanderthal genes in West African tribes like the Yoruba is one of those unexpected and unpredicted facts that on further reflection makes a lot of sense, justifying the statistical analysis used. After all, if a statistical algorithm only shows what's expected, you have to wonder whether all it's done is to give a statistical excuse for what's already believed to be true.

    Indeed, I think this is a possible explanation. On the other hand, there is just as much danger of post hoc generalization the other way!

    Testing that hypothesis will require some more sophisticated estimates of the ages of particular gene regions that have been inherited from Neandertals in West African populations.

    Tags: 
    mailbag
    Neandertal DNA
    1000 Genomes Project
    gene flow
    migration

  • Diversity doesn't point reliably to source populations

    Mon, 2011-11-07 23:08 -- John Hawks

    Worth amplifying from Dienekes' Anthropology Blog, "Y chromosomes of the Bahamas":

    I like the line about there being substantially more Y-STR variation in E1b1a7a-U174 and E1b1ba8-U175 in the Bahamas than any African collection. I have argued for years that the central assumption of phylogeography, that the location of highest Y-STR diversity is not necessarily the point of origin of a haplogroup, since Y-STR diversity can be affected both by antiquity and by admixture. Nonetheless, I keep reading papers where tiny differences in Y-STR variation, even if we forget about the noisiness of Y-STRs themselves, are taken as evidence of ancient migrations. Thankfully, the time when Y-STRs were used to infer ancient migrations is over, and the huge collection of Y-STR haplotypes amassed by population geneticists, forensic specialists, and genealogists alike can be put to uses for which it is more amenable.

    Once we have population mixture, hypotheses about phylogeography become much harder to test. A population model with mixture has many ways of generating the same pattern of relative diversity among populations.

    Tags: 
    Y chromosome
    phylogeography
    population structure
    migration

  • Mailbag: Denisovan in China and New World habitation

    Sun, 2011-11-06 14:11 -- John Hawks

    Re: "How widespread is Denisovan ancestry today?"

    Your website is so interesting I wish I were an anthropologist! The
    heat map showing interpolated spatial distribution of the frequency of
    Denisova alleles struck me - for a different reason than the subject
    of the article. Does this map add weight to the argument for a
    possible southern route for at least some of the peopling of the
    Americas? Or is it simply assumed that somehow all traces of these
    gene signatures would simply disappear during the migration from a
    northern route? I am trying to understand how this makes sense if the
    peopling of the Americas was exclusively a Northern route.

    Thanks for wonderful website.

    Not clear. The map is showing such a very small fraction of the overall genetic variation, that the similarity between the south China and central America region may be just noise. If I were to set about answering the question about New World habitation, I would start with a very different approach. Worth some consideration.

    Tags: 
    Denisova
    mailbag
    migration
    America
    China

  • Neolithic discontinuity in Hungary

    Thu, 2011-09-22 16:53 -- John Hawks

    Dienekes comments on a new paper finding another strange mixture of haplotypes in Neolithic-era sample of mtDNA from central Europe ("Unexpected ancient mtDNA from Neolithic Hungary").

    I don't think even a science fiction writer could have predicted the kinds of ancient DNA results we are getting from Europe. We have genetic discontinuity between Paleolithic and Neolithic, and between Neolithic and present, and, apparently, discontinuity between Neolithic cultures themselves, and wholly unexpected links to East Asia all the way to Central Europe.

    The paper is by Zsuzsanna Guba and colleagues [1]. The final phrase of the abstract:

    Our investigation is the first to study mutations form Neolithic of Hungary, resulting in an outcome of Far Eastern haplogroups in the Carpathian Basin. It is worth further investigation as a non-descendant theory, instead of a continuous population history, supporting genetic gaps between ancient and recent human populations.

    Past populations had incredible dynamism across Eurasia. Of course, as shown later, we need not maintain that the haplogroups presently common in East Asia have necessarily been there all that long.

    References

    1. Guba Z, Hadadi É, Major Á, Furka T, Juhász E, Koós J, Nagy K, Zeke T. HVS-I polymorphism screening of ancient human mitochondrial DNA provides evidence for N9a discontinuity and East Asian haplogroups in the Neolithic Hungary. Journal of Human Genetics. 2011.
    Tags: 
    Neolithic
    Europe
    population dynamics
    Hungary
    migration
    mtDNA migrations

  • Y chronology awry

    Wed, 2011-08-24 09:57 -- John Hawks

    Dienekes links to and discusses a current paper by George Busby and colleagues [1] on the Y chromosome chronology for the settlement of Europe: "Back to the drawing board for R-M269 (Busby et al. 2011)." The main idea is that microsatellite loci on the Y chromosome have made up the majority of our information about biogeography using this marker, but the rate of mutational changes of these loci has been badly misapplied:

    A bad clock is not useless: it gives you some information about time. Moreover, you can often use several to iron out the inaccuracy of any single one of them.

    Unfortunately, better estimation through averaging of bad estimators works only in one case: when the estimators are unbiased.

    The inclusion of some fast-mutating STR loci tends to make all estimates too young. The paper finds that this problem is general, affecting most commonly-used datasets.

    Our analysis confirms that this phenomenon is not specific to the R-M269 haplogroup nor to methods using ASD. Figure 4b shows that STRs with high D produce larger estimates of T. What is clear is that estimates of T implicitly depend on the STRs that are selected to make this inference. Using BATWING on an HGDP population for which 65 Y-STRs are available, we have shown that the median estimate of TMRCA can differ by over five times when STRs are selected on the basis of the expected duration of linearity (electronic supplementary material, figure S4). While researchers take into account STR mutation rates when estimating divergence time with ASD, commonly used STRs do not have the specific attributes that allow linearity to be assumed further into the past. The majority of haplogroup dates based on such sets of STRs may therefore have been systematically underestimated.

    One weakness of the study is that its reliance on geographic patterns of the haplotypes depends on the assumption that they have evolved neutrally relative to each other. Selection might radically affect this pattern.

    References

    1. Busby GBJ, Brisighelli F, Sanchez-Diz P, Ramos-Luis E, Martinez-Cadenas C, Thomas MG, Bradley DG, Gusmao L, Winney B, Bodmer W, et al. The peopling of Europe and the cautionary tale of Y chromosome lineage R-M269. Proceedings of the Royal Society B: Biological Sciences. 2011.
    Tags: 
    Y chromosome
    Neolithic
    Europe
    migration
    dispersal
    population structure
    recent

  • Neolithic milk fog

    Sun, 2010-10-17 14:11 -- John Hawks

    Razib points today to an article in Der Spiegel about the revival of folk migration as an explanation for the Neolithic in Europe. His post ("Völkerwanderung back with a vengeance") is worth reading. The general issues here are very interesting right now because the increase in data has made it possible to propose and test more and more complex scenarios. The simple scenario, gradual demic diffusion, appears wrong in many details. Archaeological cultures appeared and spread in spurts, which we now know were often composed of people genetically very different people.

    The article in Der Speigel is titled, "How Middle Eastern Milk Farmers Conquered Europe".

    The main idea of the article is that our understanding of the spread of Neolithic cultures into Europe has been revolutionized by ancient DNA and more sophisticated chemical analysis of artifacts. That's more or less correct. We really are thinking much more these days about folk migrations bringing new people into Europe. We know that lactase persistence was a recent evolutionary phenomenon in European groups, which was absent before the early Neolithic.

    Problem is: from the standpoint of ancient DNA samples, the lactase persistence mutation was also absent within the early Neolithic! The article is full of details that are wrong or misleading. Most important, it links the appearance and proliferation of the lactase persistence trait with the LBK. This might appear to make sense. The chemical analyses have supported the importance of dairying and presumably milk consumption in the LBK. But the genes of the LBK skeletons don't have the lactase persistence marker.

    The absence of lactase persistence in these early Neolithic people is entirely to be expected. Such an allele couldn't become common until the selection pressure was in place. People had to be drinking milk habitually at key times of vulnerability to establish this selection pressure. Even when the selection pressure is very strong, as it was for lactase persistence, the initial growth of a selected allele is very slow. It did not become common in Europe until thousands of years after it first appeared.

    So lactase persistence did not distinguish early Neolithic people in Europe from agriculturalists in the Near East, because neither of those populations had it at any detectable frequency. All the stuff in the article about how lactase persistence originated in Central Europe? It's irrelevant to whether these ancient populations were connected or not.

    What does distinguish the early Neolithic in central Europe is the mitochondrial DNA. I've discussed this several times in the last few years ("Early European mtDNA: only mysterious if you want it to be", and most recently "French Neolithic discontinuities"). The early Neolithic in Central Europe and France is characterized by several common haplogroups that are absent or rare in both earlier and later Europeans.

    It remains to be seen whether we can document a clear analogue of this mtDNA observation with nuclear genetic data. We know a lot about the variation of present-day Europeans, but most attention to geographic relationships has been run through course filters -- maps of the first two principal components are very striking in their correspondence to geography, but they really don't address the timing of movements that may have contributed to the pattern.

    The differences between early Neolithic and later Europeans suggests that post-Neolithic migrations -- real Völkerwandurung -- actually had a major impact on the European gene pool. What we see today is not a pattern established 6000 years ago, but a palimpsest richly painted with strokes from successive migrations.

    One aspect of this scenario: There's no reason to link the early Neolithic with Indo-European languages. There were many later widespread population movements that might have carried this language family, and we know that these later movements were genetically decisive -- at least, as concerns the maternal genealogy. The relation of Y chromosome haplogroups with mtDNA haplogroups is a critical question, but even more necessary is the development of an effective means of testing these hypotheses with nuclear genotype data.

    Tags: 
    migration
    Neolithic
    mtDNA migrations
    recent selection

  • "Neandertal stimulation": Weckler and biogeography

    Sat, 2010-09-25 14:27 -- John Hawks

    I'm reviewing some old viewpoints about the relationships of Neandertals and other peoples. These include mainstream opinions that persisted over decades as well as more idiosyncratic ideas. This is mostly pre-1960 stuff for the time being.

    To the extent that old ideas are wrong it is no surprise: Science progresses by rejecting wrong ideas, and paleoanthropologists of the past lacked the luxury of today's data. To the extent that the ideas look familiar, they remind us that our current hypotheses in many instances echo ideas that were advanced fifty years ago or more.

    Weckler's model

    A bit off the mainstream was a paper published by Joseph E. Weckler [1], titled "The relationships between Neanderthal Man and Homo sapiens." Weckler was a cultural anthropologist who had done fieldwork in the American Southwest and the South Pacific [2]. He wrote only one paper on Neandertals but this received substantial attention, first published in the American Anthropologist and later revised in a simplified version for Scientific American. Weckler was very interested in the migration and dispersal of ancient populations, maybe because of his work on the ethnography of the South Pacific. He brought that perspective to the Neandertals and other ancient groups.

    Weckler saw Pleistocene human population dynamics as having been directed by glaciations and geographic barriers. In general, Weckler thought that the pre-modern population had been divided into allopatric species or subspecies. These groups would have been isolated from each other much of the time, but occasionally thrust back into contact by shifts in the climate. During glacial phases, Weckler posited that Europe and Asia north of the Caucusus-Himalaya axis would have been uninhabitable. During warmer interglacials humans moved into these northern areas, where water and mountainous barriers tended to isolate them. The overall pattern was evolutionary differentiation punctuated by occasional hybridization and cultural contact between long-separated groups.

    Weckler was not the first to propose that Neanderthal and modern lineages had been relatively isolated and later hybridized. The idea was widespread after the description of the Mount Carmel remains by McCown and Keith [3]. McCown and Keith themselves had favored a different explanation -- that the Skhul and Tabun remains represented a transient between a less specialized and more specialized (Neandertal-like) extreme. Others, including Carleton Coon [4] and Theodosius Dobzhansky [5], immediately favored the idea that the Mt. Carmel sample represented a hybrid population.

    Weckler broadened the idea of hybridization into a general theme. He supposed that we might expect recurrent contact during second (Mindel-Riss) interglacial times in Central Asia, and repeated dispersal from India into Southeast Asia throughout the Pleistocene. Thus, hybridization between divergent groups was not a one-time affair but instead was a fundamental aspect of Pleistocene human evolution.

    Interglacial population contact

    This scenario faced an obvious problem: There were essentially no data to test the hypothesis of population contact at any of these earlier times. Only the third interglacial, already treated by other authors, gave the appearance of sufficient information for a test. To illustrate the plausibility of recurrent exchanges, Weckler fleshed out a third interglacial model of population contact in some detail:

    Some of these pre-Neanderthal men wandered inland into Asia north of 40° during a period of warm climate. Part of this population may subsequently have been trapped north of the barrier in the general vicinity of Inner Mongolia or Sinkiang at the onset of the next glacial period. Primitive man caught in this area would have been unable to retreat directly southward because the great mountain mass that lay in that direction became frigid sooner than the lower lands to the north. Having lived where he was for hundreds of generations, primitive man might not have known he could escape the increasingly rigorous climate by moving east several hundred miles before turning south. Howell (1951:409) suggested that some of the physical characteristics of classic Neanderthal man may represent biological adaptation to a glacial climate. Coon stated in a letter to me (1953) that he has long been of that opinion. If this is so, I suggest the evolution occurred, not in Europe during the fourth glaciation, but in eastern Asia during an earlier one (Weckler 1954:1010).

    This is an early exposition of the idea that Neandertals repeatedly invaded the west from a homeland somewhere in central Asia or further east. Weckler discussed the idea that these populations originated in northwestern China, but he had no good examples (as indeed there are still no such examples).

    Weckler's discussion may seem confused because he accepted Zhoukoudian as an eastern "Neanderthaloid" population. His division of humanity can best be aligned along a "paleanthropic/neanthropic" distinction. Today, we might more simply state his biogeographic model as a shifting border between the paleanthropic "Neanderthaloids" and neanthropic "Homo sapiens" along a shifting Movius line somewhere in India or the Middle East, stretching to northwestern China.

    A central Asian source

    Teshik Tash bears much importance to Weckler's ideas, as it did to Movius, Howell, Weidenreich, and many others. To those unfamiliar with the site, an interesting place to start is my interview with Mica Glantz. Teshik-Tash is once again central to our ideas of Neandertal biogeography, with the addition of genetic evidence from the juvenile specimen from the site and others in Central Asia.

    In the early 1950s, Teshik-Tash raised many of the same issues that it does today. Today, of course, Teshik-Tash is far from alone, with several sites in Central Asia bearing evidence of a local Mousterian, physical remains with Neandertal-like mtDNA sequences. There was great uncertainty about the date represented by the Teshik-Tash specimen. Teshik-Tash had a classic "Western" archaeological industry (in this case, Mousterian) and therefore evidenced long-range population contact with Europe. The East Asian fossil record was known to be very different from the west, raising the question of boundaries. Where did the Western sphere of biological influence end, and the Eastern begin?

    Today Denisova Cave, embedding a highly divergent mtDNA clade in an initial Upper Paleolithic assemblage [6], presents the same issues with even greater relief.

    Probably the most common interpretation of the Central Asian "Neandertal" sites is that they represent an eastward migration from the Neandertals' center of evolution in Europe. But the opposite hypothesis is an obvious alternative: that the center of Neandertal evolution was somewhere in Central Asia, and that they invaded Europe from outside. Some may see parallels for a Neandertal invasion of Europe from outside, by looking both earlier in evolution (the first Europeans obviously came from somewhere) and later (the Upper Paleolithic, the Neolithic).

    Why posit Central Asia in particular as a source area, above and beyond the general idea of invasion? I thought the idea might have originated with Henry Fairfield Osborn because of his long interest in Central Asia as a center of human evolution. For Osborn, Central Asia was a source of humanity, but his "Dawn Man" idea supposed that the modern human form had long resided in Central Asia, with more primitive humans at the periphery. The idea that a Neandertal center of evolution existed in Asia is quite different from Osborn's idea, which was itself a sketch supported by little evidence. I'll have more on Osborn later.

    Weckler presented his idea to address a classic problem: To many paleoanthropologists, early Neandertals appeared to be more like later human than were the later, "classic" Neandertals. Howell [7] summed up this observation as follows:

    Many features of early Neanderthal morphology, both cranial and postcranial, are incipiently classic Neanderthal. However, the general morphological pattern of these early Neanderthal peoples bore a close resemblance to that of anatomically modern man, a fact which indicates again the special character of classic Neanderthal morphology (Howell 1957:332-333).

    The early Neandertals were those from the third interglacial, which during the 1950's would have included those from Krapina, Ehringsdorf, and Saccopastore. Howell's description highlights the most common hypothesis: classic Neanderthals had evolved toward greater and greater specialization over time.

    Weckler took a different approach: for him, the fourth glaciation Neandertals descended from already-specialized ancestors, who had existed in Central Asia:

    The Asiatic migrants, probably already mixed with Homo sapiens in central Asia in the Middle East, pushed on to central Europe during the third interglacial. They may have moved northwestward from Palestine or directly westward along the north face of the barrier. In the zone of contact in western Asia and eastern Europe further miscegenation and cultural exchange probably occurred. Then, when the climate deteriorated with the onset of the fourth glaciation, the bulk of the Homo sapiens population retreated south as was its wont. This left Europe open to further Neanderthal invasion and set the stage for the modern misconception that classic Neanderthals evolved rapidly (and in a curiously regressive fashion) in western Europe during Würm I. Probably all that actually happened was that additional Neanderthals of more classic type, adjusted by previous experience to life in a cold climate, kept pushing in behind the advance guard and, by weight of numbers, blotted out the neanthropic traits the earlier migrants had acquired along the way.

    Weckler proposed this scenario not long after F. Clark Howell's 1952 paper [8], in which Howell had proposed that climate isolated Neandertals within Europe during the last glaciation, leading to their increasing specialization. According to Weckler, the glaciations had not isolated Europe so much as they had wiped clean the evolutionary slate within Europe. After the last interglacial, migration from a central Asian source brought back a purer strain of Neandertal.

    Out of this welter of fact and interpretation emerge the few concepts necessary to the hypothesis supported in this paper. By the end of third glacial times Neanderthal had probably developed in eastern Asia to something approximating the classic form. His numbers had probably always been small compared to developing Homo sapiens: his range was incomparably smaller, and in part of this range he had no easy retreat from glacial conditions such as Homo sapiens enjoyed. His restricted range (and possibly his sometimes severe habitat) had militated against the racial diversification that characterized the development of Homo sapiens. In spite of his cultural advances his range and numbers were probably sharply reduced during every glacial episode he had to endure. This may be why, although he stood athwart the entrance to the New World, he never expanded his range sufficiently to explore that territory. But as the climate ameliorated after the rigors of the third glaciation, his numbers increased and he did finally expand his range. For reasons not as yet ascertained he looked westward, and the lowlands north of the barrier afforded him a route to Europe.

    Several strains of contemporary thought emerge in Weckler's formulation. Neandertals were always on the edge of extinction, being repeatedly driven to low numbers by deteriorating climate. Their tenuous existence did not allow them to disperse more broadly.

    That old Neandertal magic

    Where Weckler differed from the received view is in the way he accentuated the Neandertal positives. He wrote that the diversification of humans and Neandertals presented an opportunity to the evolution of our species. From their central Asian source, the Neandertals had acquired innovations necessary for existence in the cold north. Human colonization of these regions might be impossible without the adoption of Neandertal cultural and behavioral innovations:

    The Homo sapiens groups that retreated south from Europe and perhaps from central Asia [during the glaciation] had been touched by Neanderthal magic. They may have acquired some Neanderthal physical traits, but, more important, they had achieved a new cultural outlook. They had perhaps learned the use of fire, clothing and specialized hunting techniques, and possibly of cave dwelling -- accomplishments that freed man from dependence on a mild climate and from a grubbing existence (emphasis added).

    I find myself reading this on two levels. On the concrete, empirical side, Weckler would soon be proven wrong. Neandertals didn't invent fire; that was much older and more broadly shared by Middle and Late Pleistocene humans. They may have had better clothes for cold weather than contemporaries who lived further south, but the innovations of woven cloth, sewn garments, and shoes happened later. They certainly had specialized hunting techniques, but these were linked to a particular kind of social organization and technology. Later developments in both would have required new hunting (and gathering) methods. None of them lived in caves very often; their experience must have been fairly "grubbing" in either event.

    But on the abstract, Weckler presents a scenario where Neandertals had something of value, cultural or physical, without which later humans would have been as successful. He had already posited biological hybridization; here he suggests a kind of "cultural hybridization" as well.

    The essential idea I am suggesting is that the contact of Homo sapiens groups with "Neanderthal culture" in Asia and in Europe during the third interglacial resulted in an efflorescence of "Homo sapiens cultures" that gave rise to the Upper Paleolithic. There is general agreement, I think, that a sudden enrichment of culture is evident at the beginning of the Upper Paleolithic in Europe and that these richer and more varied cultures seem to have originated, for the most part, outside of Europe. Movius, discussing the European Upper Paleolithic (1953:171ff.), follows M. Denis Peyrony, Dorothy Garrod, and others in suggesting that different European cultures of that time may have originated in Palestine, Iran, the plains of southern Russia, and possibly Africa. All but the latter are areas where indigenous Homo sapiens was probably directly stimulated during the third interglacial by invading Neanderthal man (Weckler 1954:1016).

    So why has this idea been largely forgotten? The failure of the particulars was almost complete:

    Leakey claimed in the 1930's that Lower Aurignacian techniques of stone chipping were older in Africa than in Europe (1931:237-39; 1936:54-60, 161). Movius seems ready to dismiss Africa as a source of European Aurignacian (1953:171), but he doesn't dispose of Africa's claim to temporal priority. The sudden new competence Leakey claims for African Aurignacian cultures early in the fourth glaciation (1936:161) may have been the consequence of contact with Neanderthal. The stimulation may have come secondhand from Homo sapiens wanderers returning from Europe or may have resulted directly via diffusion or migration from the Middle East.

    He was overreaching here. He didn't overestimate the cultural sophistication of Neandertals, although he did accentuate behaviors, like fire, that would turn out to be less special than he assumed -- older than Neandertals and more broadly shared. More critically, Weckler rested his argument on the absence of evidence for cultural sophistication in the African contemporaries of the Neandertals. But Louis Leakey's earlier claims about an "African Aurignacian" also overreached, supported by a mistaken chronology. A better understanding of the Late Pleistocene African cultural sequence would emerge only later.

    When Homo sapiens had thoroughly assimilated and improved on the ideas he got from Neanderthal, he took advantage of the first interstadial of the Würm glaciation to launch forth on his initial conquest of the world. He overran Europe and pushed around the barrier into eastern Asia.... One might even hazard the guess that the reason Africa south of the Mediterranean littoral remained so backward during the Upper Paleolithic was because the Homo sapiens groups there had not had the full benefit of Neanderthal stimulation. In the new dynamics of cultural enrichment and sapiens migrations the hinterlands of Africa had become a dead end, far removed from the centers of rapid development.

    I find myself wondering about the nature of "Neanderthal stimulation"....

    This passage is worth examination. Most of the details have changed radically since 1954. We now know that MSA Africans had most of the tricks that Neandertals did, and vice-versa. Many MSA industrial innovations predate Mousterian or Middle Paleolithic occurrences. The complexity within Africa may itself represent a vastness of population history that we now can only guess at.

    Yet the development of Upper Paleolithic cultural complexity still wants some explanation. The biological innovation of "anatomical modernity" is not sufficient to explain the cultural evolution of the Late Pleistocene -- it does not match the pattern of cultural innovation in time or space.

    Bottom line

    I think there was some "Neandertal magic." Middle Pleistocene humans were more isolated than present-day populations, for a longer period of time. Less gene flow made it less likely for adaptive traits to spread beyond the population where they originated. Not impossible, just less likely. So any surge of population contact caused by migration would have been accompanied by a surge of introgression of adaptive genes. The evidence for Neandertal contribution to the later gene pool of non-Africans documents one such surge of population contact, but there may well have been others.

    Where genes are concerned, this is a simple matter of mathematics, discussed more fully by Greg Cochran and I in our 2006 paper [9]. Simply put, Neandertals and modern humans had comparable selection pressures for many aspects of their biology, similar adaptive responses, and the same time to adapt. Adaptive mutations are chance events, governed by demography and time. If the evolving African MSA population got many new adaptive mutations, Neandertals would have gotten nearly as many (possibly constrained by smaller population size). In a few cases, the same variants would occur in both populations by chance, but in most they would be different. These alleles should still be with us, as the extent of Neandertal contribution to our population was great enough to pick up almost all of them.

    But what about Neandertal cultural traits? These were the real focus of Weckler's argument, and here I think the question is very difficult to resolve today. Cultures are ephemeral. As we know from history, if we choose a beginning and end point a few hundred years apart, it can be difficult to show the continuity of cultural information even within a single place.

    With the transition from Mousterian, through Châtelperronian into Aurignacian in France and northern Spain -- a place where we have relatively dense archaeological documentation -- we are nevertheless talking about time gaps of hundreds of years. I'm skeptical that we're in a position to test the hypothesis of cultural exchanges across these time periods.

    We're in a better position to test the hypothesis of stasis. If genetic exchanges happened in the absence of culture change, that would tell us something very relevant to the relation between gene flow and demographic contact. Likewise, persistent stasis of different cultures in adjacent areas tells us something about the absence of information flow. A kind of regional stasis, over thousands of years, seems to have been the norm in MSA and Middle Paleolithic contexts, and it's not a pattern that we are well-placed to understand without a better understanding of the limits on information exchange. Some of those limits may, in these ancient populations, have been biological constraints. So I'm less confident that we will be able to understand the cultural consequences of Neandertal contact.

    References

    1. Weckler JE. The Relationships Between Neanderthal Man and Homo sapiens. American Anthropologist. 1954;56:1003–1025.
    2. Hoijer H. Joseph Edwin Weckler, Jr. 1906-1963. New Series [Internet]. 1964;66:1348–1350. Available from: http://dx.doi.org/10.2307/667992
    3. McCown TD, Keith A. The Stone Age Man of Mount Carmel: The Fossil Human Remains from the Levalloiso-Mousterian. Oxford: Clarendon Press; 1939.
    4. Coon CS. The Races of Europe. New York: MacMillan; 1939.
    5. Dobzhansky T. On species and races of living and fossil man. American Journal of Physical Anthropology. 1944;2:251–265.
    6. Krause J, Fu Q, Good JM, Viola B, Shunkov MV, Derevianko AP, Paabo S. The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature [Internet]. 2010;464:894–897. Available from: http://dx.doi.org/10.1038/nature08976
    7. Howell FC. The evolutionary significance of variation and varieties of "Neanderthal" man. The Quarterly Review of Biology. 1957;32:330–347.
    8. Howell FC. Pleistocene glacial ecology and the evolution of "Classic Neandertal" man. Southwest Journal of Anthropology. 1952;8:377–410.
    9. Hawks J, Cochran G. Dynamics of Adaptive Introgression from Archaic to Modern Humans. PaleoAnthropology. 2006;2006:101–115.
    Tags: 
    Neandertal DNA
    history of anthropology
    hybridization
    extinction
    climate
    introgression
    Neandertals
    migration
    paleoclimate
    Synopsis: 
    A 1954 paper expresses a very modern perspective on climate and Neandertal evolution

  • French Neolithic discontinuities

    Sun, 2010-08-22 19:47 -- John Hawks

    Marie-France Deguilloux and colleagues [1] present a short analysis of ancient mtDNA recovered from a Neolithic burial at Prissé-la-Charrière, between the Loire and Garonne valleys of western France.

    The mtDNA sample in the end was only three individuals -- one haplogroup X2, one U5a and one N1a. Each is intriguing, as far as a single sequence can be, because all are rare or absent from France today. I think one shouldn't go far interpreting three samples, but they contribute to the view that Neolithic mitochondrial variation in Europe was very different from recent Europeans. The N1a and U5b sequences fit within the already-known Neolithic (and for U5a, Mesolithic) variation in central and northern Europe.

    It is from the U5a that Deguilloux and colleagues make a point about possible Mesolithic population continuity.

    Subhaplogroup U5b has also been encountered in German Neolithic remains from the Corded Ware Culture (Haak et al., 2008) and in the hunter-gatherers studied by Bramanti et al. (2009), although in both instances, the branches concerned were distinct from the U5b in the Prissé sample. It is, however, worth noting that haplogroup U5 has been encountered in surprising frequency in the hunter-gatherers studied by Bramanti et al. (2009) and could correspond to a Mesolithic heritage.

    The story of N1a is that it was very common in the central European Neolithic, even though it is very rare today. That was first noted by Wolfgang Haak and colleagues [2], and has in subsequent years been joined by the observation that the pre-Neolithic hunter-gatherers had yet other common haplogroups. The population history of Europe was a lot more interesting than we suspected 10 years ago.

    Deguilloux and colleagues attempt a conservative explanation for the frequencies of N1a in Neolithic samples:

    The widespread distribution of the N1a lineage in Early and Middle Neolithic northwestern Europe may indicate genetic continuity from Mesolithic populations. This scenario would support a Mesolithic contribution to the earliest Neolithic of Atlantic Europe. This would imply that the N1a lineage was already common in indigenous north European populations and that the spread of the Neolithic was principally the result of cultural diffusion. Although so far the N1a lineage has not been encountered among late European hunter-gatherers in central and north Europe (Bramanti et al., 2009; Malmström et al., 2009), it is worth noting that less than half of the hunter-gatherers' paleogenetic data come indeed from the pre-Neolithic period (predating LBK expansion). Finally, no paleogenetic data currently exist for the Mesolithic period in Western Europe. This prevents any conclusion being drawn about N1a occurrence during the Mesolithic period in those regions.

    I will note this -- the more that N1a is replicated across the Neolithic of Europe, the less and less likely that its subsequent vast reduction in frequency could result from genetic drift. When there was only one or two samples from Central Europe with high N1a, it was at least possible that this was a local founder population that did not spread its mtDNA diversity very far. If it were localized, even in the central Danube (a fairly big region) it might be possible to maintain that the later decline of N1a to its present low frequency had been due to population replacement.

    Now N1a seems like a real marker of the LBK, spread widely into Western Europe. It may be, as Deguilloux and colleagues suggest, that it will be found at substantial frequencies in earlier samples somewhere in Europe. We do want some explanation for how it got to be common in this culture area.

    Dienekes has written about the study. His point is a good one: If N1a were present somewhere in pre-Neolithic Europe, it would require some kind of "partition" of the pre-Neolithic population, along with its propagation -- presumably southeastward -- into the LBK of central Europe. Seems doubtful.

    The study includes an illuminating paragraph about the sources of contaminating sequence in these Neolithic extractions.

    Strict precautions were followed during all procedures (including precautions during excavation) and proved to be effective, because all researchers who directly participated in this study (from people working in the field to those working in the laboratory) were genotyped and their sequences were never observed during analyses. However, European sequences were randomly found in clones (28% of the sequences obtained). These specific sequences are regularly observed in the laboratory, whatever the project tackled (including samples from Polynesia or South America), in clones from samples or negative controls. They are not reproducible for a specific sample and are different from researchers' sequences. These facts lead us to suspect the contamination of PCR reagents (Leonard et al., 2007). It was relatively easy, however, to discard those contaminating sequences from our analyses because they were largely in the minority when compared with endogenous sequences.

    It would not be very difficult to compare the results from different labs and do a forensic-quality analysis of these reagent contamination events. Surely a good fraction of ancient DNA results prior to the last few years must represent such contamination. Nowadays people have the expectation that Neolithic-era remains may have rare or exotic haplogroups, but it hasn't been so long since people assumed that French equals French. I expressed some concern about this criterion before -- "strange" stands in for "non-contaminated" in too many studies.

    It might be very helpful to have a paper outlining the actual contamination pathways that have been found to affect multiple labs. Then the results could be compared against reports that have come out over the years. If people are reluctant to cull doubtful ancient DNA results, at the very least they can target a set for replication studies.

    References

    1. Deguilloux M-F, Soler L, Pemonge M-H, Scarre C, Joussaume R, Laporte L. News from the west: Ancient DNA from a French megalithic burial chamber. Am. J. Phys. Anthropol. [Internet]. 2011;144:108–118. Available from: http://dx.doi.org/10.1002/ajpa.21376
    2. Haak W, Forster P, Bramanti B, Matsumura S, Brandt G, Tänzer M, Villems R, Renfrew C, Gronenborn D, Alt KW, et al. Ancient DNA from the First European Farmers in 7500-Year-Old Neolithic Sites. Science [Internet]. 2005;310:1016–1018. Available from: http://dx.doi.org/10.1126/science.1118725
    Tags: 
    population history
    Upper Paleolithic
    France
    mtDNA
    Neolithic
    population structure
    Europe
    migration
    mtDNA migrations
    Synopsis: 
    Study of mtDNA from a Neolithic-era burial in France contributes to an overall picture of Neolithic population replacement in Europe

  • Migration thinking

    Fri, 2010-08-20 08:30 -- John Hawks

    Murray Cox and Michael Hammer have a short commentary piece in the current BMC Biology, titled, "A question of scale: Human migrations writ large and small" [1]. They review a few recent papers concerning human migration and intermixture -- including the Neandertal genome draft [2], the paper by Chuanxiang Li and colleagues showing Bronze Age admixture in the Tarim Basin [3], and their own work quantifying historical gene flow inside and outside Africa [4].

    It's a short review, but I thought their conclusion serves some thought -- they discuss some of the theoretical complexity of estimating ancient rates of gene flow. The simple model assumes constant rates, but human populations aren't simple.

    We expand on just one of these points for illustration (Figure 3). Even when gene flow is inferred explicitly, existing methods invariably assume that it has remained constant through time. However, it seems more reasonable that two diverging populations might share more migrants initially (due to shared geography or existing social relationships), with gene flow subsequently decreasing exponentially as the two populations move apart (Figure 3a). Or gene flow might increase exponentially as two geographically separated populations begin to move closer together (Figure 3b). Alternatively, gene flow might suddenly resume between two long separated populations; for instance, where geographically disconnected populations came back into contact, either as hunter-gatherer groups during the late Pleistocene (Figure 3d), or as human mobility increased following the development of farming in the Holocene (Figure 3c). The important point is this: two populations can look very similar (FST = 0) or very different (FST = 0.3) even when they have exchanged the same number of migrants (that is, graph lines with the same color in figure 3). It is therefore insufficient to consider only how many migrants have moved between populations; we also need to know when these movements occurred.

    I don't reproduce the figure, because it's complicated and I think the text is sufficient to establish the point. Averages aren't very meaningful. I'll point out that there is some hope of testing these hypotheses, if we consider selected genes -- which have a time that they originated.

    References

    1. Cox M, Hammer M. A question of scale: Human migrations writ large and small. BMC Biology [Internet]. 2010;8:98+. Available from: http://dx.doi.org/10.1186/1741-7007-8-98
    2. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, et al. A Draft Sequence of the Neandertal Genome. Science [Internet]. 2010;328:710–722. Available from: http://dx.doi.org/10.1126/science.1188021
    3. Li C, Li H, Cui Y, Xie C, Cai D, Li W, Mair V, Xu Z, Zhang QC, Abuduresule I, et al. Evidence that a West-East admixed population lived in the Tarim Basin as early as the early Bronze Age. BMC Biology [Internet]. 2010;8:15+. Available from: http://dx.doi.org/10.1186/1741-7007-8-15
    4. Cox M, Woerner A, Wall J, Hammer M. Intergenic DNA sequences from the human X chromosome reveal high rates of global gene flow. BMC Genetics [Internet]. 2008;9:76+. Available from: http://dx.doi.org/10.1186/1471-2156-9-76
    Tags: 
    population genetics
    gene flow
    migration
    population dynamics
    China
    metapopulations
    Neandertal DNA

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