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A few years ago a paper was published, Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins, in PNAS, which argued that ancient population structure within Africa might be the reason that non-African populations are genetically closer to Neandertals. The basic logic is simple. If within Africa there was variation in relatedness to Neandertals, and modern non-Africans are derived from the group that was closer to Neandertals, then one might infer that there was recent admixture between the groups even though any connection was very distant in the past. This objection actually popped up immediately when the Neandertal admixture Science paper was published. Over time many people have been convinced by various ingenuous and abstruse arguments.

The problem is that not everyone is a statistical geneticist, nor do they think about these issues very often. When it comes to the media they have to rely on what’s being published in prominent journals. The PNAS paper above has haunted the field in my opinion, because reporters have had to take the researchers at their word, when frankly most statistical geneticists that I know did not find their arguments very persuasive in the first place. Today we have even less reason to believe them. A few hours ago I saw this in my feed from the Genetic Literacy Project, More mystery about Neanderthal and modern humans: How reliable is ancient DNA analysis? The answer is very reliable. There’s no controversy.

The figure at the top of this post is from Genome sequence of a 45,000-year-old modern human from western Siberia. What you see is that the markers diagnostic of Neandertal ancestry are clustered together in segments to a far greater extent in the ancient sample than among modern peoples. This sort of pattern of decaying tract length is a hallmark of pulse admixtures. Each generation recombination breaks apart associations until the tract lengths are very small (or, they are not detectable). There are now at least two ancient samples which show that Neandertal-modern human admixture occurred in the relatively recent past in relation to their own period in comparison to modern individuals. That in itself reduces the probability of ancient structure being the dominant explanation for the Neandertal affinities of non-Africans, as ancient structure would not exhibit this tract length bias. And, this result has the utility of being amenable to common sense comprehension.

• Category: Science • Tags: Neandertal 
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250px-Caveman_1 By now you may have heard that mitochondrial DNA, passed down the female lineage, has been extracted from a ~400,000 year old human fossil from Spain. If you haven’t heard, I recommend Ewen Callaway and Carl Zimmer’s takes. The paper is at Nature, so gated, A mitochondrial genome sequence of a hominin from Sima de los Huesos. The big surprise is that these proto-Neandertals carry a mtDNA lineage which is closer to that of the Siberian Denisovans than that of later Neandertals. That’s the specific finding, and if you read the reaction it is rather clear that this is confusing researchers who work in this area. But take a step back, imagine what a world without ancient DNA would be like. Yes, the broad conjectures would be supported (e.g., Out of Africa), but many specific details would be off. So praise the data! Sometimes complexity is closer to the truth, and this is one of those cases. These are good problems to have.

Neander In the primary figure of the paper you can see that these humans are closest on the mtDNA phylogenetic tree to the Denisovans. But, it is important to note that they’re also hundreds of thousands of years older than any other ancient human DNA. Because mtDNA is only passed down through females it tends to be more strongly subject to genetic drift, which might turn over lineages rather rapidly. It is not that unlikely that over hundreds of thousands of years some populations would lose ancestral mtDNA lines. This is what occurred with “mitochondrial Eve.” She wasn’t the only female alive in Africa at the time, but all the other direct maternal lineages went extinct. There are ‘ghost branches’ within the tree which terminated. All you see are the lines of descent back up to the single last common ancestor on the mitochondrial lineage. This doesn’t mean that the ancestry of these women who did not contribute mtDNA disappeared. It is just that their lines of descent may have passed through sons at a given point (my maternal grandmother’s specific mtDNA almost went extinct, she had six son and one daughter). And of course there are other explanations for this pattern, highlighted in the articles linked. Gene flow between lineages, or from a different lineage altogether. We have to remember that the mtDNA of the Denisovan human was more diverged from Neandertals than the whole genome was later found to be, perhaps indicating complex admixture scenarios. The mtDNA tree falsifies, but I do not think it allows us to draw any robust conclusions.

These results are going to get updated in the next year or so with autosomal DNA from the rest of the genome. Even if they can’t get the whole genome sequenced, even a few tens of thousands of markers should be sufficient to clarify issues. Though all of these findings need to be interpreted cautiously in light of the fact that this is a very old lineage, perhaps closer to the time period of diversification for many Eurasian ‘archaic’ H. sapiens than we may have thought.

• Category: Science • Tags: Denisovan, Neandertal, Paleoanthropology 
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With all the crazy talk about George Church and an adventurous young woman conspiring to bring back Neandertals, I do think it is important to keep in mind that we can bring back an individual with a predominantly Neandertal genome in a very old fashioned manner: controlled breeding. The most humane and viable manner in which you might do this is simply start a religion in a Bene Gesserit fashion where the prophesied Kwisatz Haderach is a Neandertal. Over the generations by selecting individuals within the population (which could draw in converts) enriched for Neandertal ancestry to mate assortatively one could slowly increase the proportion of that ancestral component. The population would become more and more “Neandertal,” probably to the point of being phenotypically distinctive in a dozen generations (even a minority of non-modern human ancestry is probably significant, just as many individuals who are 3/4 European and 1/4 African still exhibit features of their minority heritage). One could apply the same logic to the Denisovans.

I think this obviates the bioethical concerns, as a natural group of Neandertals would emerge over time in an organic fashion. At least in a genomic sense (though likely there will always be “gaps” in the reconstructed genome; for example the mtDNA). One might object that one can’t bring back Neandertal culture, but it strikes me as patronizing and peculiar to presume that Neandertals (in a genomic sense) should exhibit a biocultural integrity that we don’t expect from the descendants of anatomically modern humans. No doubt ever generation young Neo-Neandertals would leave the cultish environs of their natal sect. Perhaps there would be apostate Neo-Neandertals making the hajj. Kissing the ring of the Pope in Rome. Retreating to Fiji to paint the native modern humans.

You might think this is a farcical suggestion, but why not? Today we live in the world of individual self-actualization and hedonic utilitarians. In short, we live as individuals to wallow in our own pleasure. Why not look deep into the future, perhaps beyond our own mortality? The resurrection of assimilated hominin lineages would be a noble artistic experiment. Even if the revived lineages are clearly different in fundamental ways, it would add to the diversity of the world. Is in a sin that they would “think different”?

• Category: Science • Tags: Anthropology, Human Genomics, Neandertal 
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Birds of a Feather: Neanderthal Exploitation of Raptors and Corvids:

The hypothesis that Neanderthals exploited birds for the use of their feathers or claws as personal ornaments in symbolic behaviour is revolutionary as it assigns unprecedented cognitive abilities to these hominins. This inference, however, is based on modest faunal samples and thus may not represent a regular or systematic behaviour. Here we address this issue by looking for evidence of such behaviour across a large temporal and geographical framework. Our analyses try to answer four main questions: 1) does a Neanderthal to raptor-corvid connection exist at a large scale, thus avoiding associations that might be regarded as local in space or time?; 2) did Middle (associated with Neanderthals) and Upper Palaeolithic (associated with modern humans) sites contain a greater range of these species than Late Pleistocene paleontological sites?; 3) is there a taphonomic association between Neanderthals and corvids-raptors at Middle Palaeolithic sites on Gibraltar, specifically Gorham’s, Vanguard and Ibex Caves? and; 4) was the extraction of wing feathers a local phenomenon exclusive to the Neanderthals at these sites or was it a geographically wider phenomenon?. We compiled a database of 1699 Pleistocene Palearctic sites based on fossil bird sites. We also compiled a taphonomical database from the Middle Palaeolithic assemblages of Gibraltar. We establish a clear, previously unknown and widespread, association between Neanderthals, raptors and corvids. We show that the association involved the direct intervention of Neanderthals on the bones of these birds, which we interpret as evidence of extraction of large flight feathers. The large number of bones, the variety of species processed and the different temporal periods when the behaviour is observed, indicate that this was a systematic, geographically and temporally broad, activity that the Neanderthals undertook. Our results, providing clear evidence that Neanderthal cognitive capacities were comparable to those of Modern Humans, constitute a major advance in the study of human evolution.

Not to be too skeptical, but has anyone done an analysis of a possible change in the nature of publications about the cognitive capacities of Neandertals since it was established that there is a high likelihood of admixture between that lineage and ours (i.e., that that lineage is to some extent ours)? This is where I have to point to Luke Jostins’ loess curve illustrating the increase in cranial capacity of hominins over the past few million years. As Luke notes “brain size increases gradually in all lineages.”

This isn’t to deny that there seem some qualitative differences between the descendants of anatomically modern humans and other hominins. Neandertals, Denisovans, etc., never made it to the New World or Oceania. But there are differences, and there are differences. One model which was rather popular, and which I tacitly accepted, is that modern humans, the “descendants of Eve,” are sui generis. Somehow, somewhere, ~50-100,000 years ago a lineage of geniuses came upon the scene and swept all others away. I don’t accept this proposition anymore. Rather, it may be that 1-2 million years ago the hominin lineages took some irreversible step, and all the parallel and reticulate branches were hurtling toward a new evolutionary equilibrium.

• Category: Science • Tags: Evolution, Neandertal 
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Neandertal ancestry “Iced”:

Evaluating recent evolution, migration and Neandertal ancestry in the Tyrolean Iceman

Paleogenetic evidence from Neandertals, the Neolithic and other eras has the potential to transform our knowledge of human population dynamics. Previous work has established the level of contribution of Neandertals to living human populations. Here, I consider data from the Tyrolean Iceman. The genome of this Neolithic-era individual shows a substantially higher degree of Ne- andertal ancestry than living Europeans. This comparison suggests that early Upper Paleolithic Europeans may have mixed with Neandertals to a greater degree than other modern human populations. I also use this genome to evaluate the pattern of selection in post-Neolithic Europeans. In large part, the evidence of selection from living people’s genetic data is confirmed by this specimen, but in some cases selection may be disproved by the Iceman’s genotypes. Neolithic-living human comparisons provide information about migration and diffusion of genes into Europe. I compare these data to the situation within Neandertals, and the transition of Neandertals to Upper Paleolithic populations – three demographic transitions in Europe that generated strong genetic disequi- libria in successive populations.

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Yesterday I pointed out that David Reich had a moderately dismissive attitude toward the new paper in PNAS, Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins. Here’s what Reich said:

…But Reich believes that the discussion would have been different if it had happened in the open. The PNAS paper questioning the Neanderthal admixture addresses issues swirling around two years ago, but not Reich and Slatkin’s latest work. “It’s been an issue for several years. They were right to work on this,” says Reich. But now, “it’s kind of an obsolete paper,” he says.

Here’s what Nick Patterson, Reich’s colleague told me via email:

Ancient structure in Africa was considered when we wrote the Green et al. paper, and we were aware that this could explain D-statistics. But the hypothesis is no longer viable as the major explanation of Neandertal genetics in Eurasia. This was discussed in the recent paper of Yang et al. (MBE, 2012). (Not referenced by the PNAS paper).

A very simple argument, that convinces me, is that the allelic frequency spectrum of Neandertal alleles in Eurasia falls off very quickly. A bottleneck flattens out the spectrum, and it turns out that the Neandertal gene flow has to be placed after the out of Africa bottleneck or the spectrum is much too flat.

The paper on the arXiv from the Reich lab (Sankararaman et al.) is trying to do something much more subtle than this and date the flow. I personally am no longer interested in explaining the introgression as ancient structure. That ship has sailed.

Of course the question of what was the genetic structure of Ancient Africa is quite open, and remains very interesting.

If Nick’s explanation is a bit cryptic for you (he was a cryptographer!), figure 2 from the Yang et al. paper lays it out quite clearly:

Let’s back up for a moment and set the stage. What did they do in the PNAS paper which claims that one can not reject the model that the Eurasian affinity to Neandertals is due to ancient African population structure (i.e., the African ancestors of Eurasians already had a closer affinity to Neandertals, perhaps due to continuous gene flow)? Basically they created an explicit spatial model with a temporal dimension. The authors simulated parameters of gene flow (and lack thereof) as well as bottlenecks, etc., and found that ancient structure easily generated the D-statistic which the original authors of the Neandertal admixture paper relied upon.

So why so dismissive from Reich & Patterson? Because the Yang et al. paper admits this problem, and formulates a way to test alternative scenarios which generate just those D-statistics, but exhibit different demographic histories. What they found in Yang et al. is that a model where a population bottleneck occurs followed by admixture is the best fit to the site frequency spectrum that you see in real populations today. In other words, they also simulated situations where ancient structure generated equivalent D-statistics to admixture, and then furthermore explored scenarios where other population genetic statistics could further prune the alternatives. One could say that the appropriate follow up paper to the PNAS contribution was actually published before it.

The paper on arXiv (to be published in PLoS Genetics) goes much further. Using patterns of the linkage disequilibrium in the genome they produce a date when the admixture occurred. The statistical genetics here is somewhat opaque to the casual reader, so interpretation of these results probably should be conditional on the Yang et al. paper, whose results are more elegant and easy to digest.

After all is said and done David Reich’s judgment is not atypical. Several people who I know personally and are deeply immersed in human population genomics are simply not impressed by the PNAS paper. That happens, and there’s no shame in it. But Reich has a point: a speedier process of publication and review would have saved a lot of people some energy.

Related: Dienekes’ comments.

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Dienekes tips me off to the fact that the long-awaited Reich lab paper on Neandertal admixture dating has finally been put on arXiv! The date of interbreeding between Neandertals and modern humans:

Comparisons of DNA sequences between Neandertals and present-day humans have shown that Neandertals share more genetic variants with non-Africans than with Africans. This could be due to interbreeding between Neandertals and modern humans when the two groups met subsequent to the emergence of modern humans outside Africa. However, it could also be due to population structure that antedates the origin of Neandertal ancestors in Africa. We measure the extent of linkage disequilibrium (LD) in the genomes of present-day Europeans and find that the last gene flow from Neandertals (or their relatives) into Europeans likely occurred 37,000-86,000 years before the present (BP), and most likely 47,000-65,000 years ago. This supports the recent interbreeding hypothesis, and suggests that interbreeding may have occurred when modern humans carrying Upper Paleolithic technologies encountered Neandertals as they expanded out of Africa.

This isn’t the only group working on the Neandertal genomic admixture story. From reading his blog you probably know that John Hawks is working in this area, but there are other labs too. I’m hoping that the Reich lab pushing their stuff on arXiv will prompt the other groups to also start moving (instead of just presenting preliminary results to a narrow group of researchers).

As for these results, I’m still amazed that LD based methods can work this far into the deep past. Second, it is nice that the low bound estimate can plausibly predate the arrival of anatomically modern humans to Australia. Also, this admixture date is well after anatomical modern humanity, and well before the classical “Great Leap Forward” of behavioral modernity. Though I think that over the next few years we may start to discard the idea of any such punctuated leap.

And again, it’s on arXiv. As they used to say, read the whole thing!

• Category: Science • Tags: Human Evolution, Neandertal 
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An interview with paleoanthropologist Chris Stringer:

This raises one more question: Could we ever clone these extinct people?

Science is moving on so fast. The first bit of Neanderthal mitochondrial DNA was recovered in 1997. No one then could have believed that 10 years later we might have most of the genome. And a few years after that, we’d have whole Denisovan and Neanderthal genomes available. So no one would have thought cloning was a possibility. Now, at least theoretically, if someone had enough money, and I’d say stupidity, to do it, you could cut and paste those Denisovan mutations into a modern human genome, and then implant that into an egg and then grow a Denisovan.

I think it would be completely unethical to do anything like that, but unfortunately someone with enough money, and vanity and arrogance, might attempt it one day. These creatures lived in the past in their own environments, in their own social groups. Bringing isolated individuals back, for our own curiosity or arrogant purposes, would be completely wrong.


I do find it curious that Chris used the term “creatures.” This probably not intentional, or with serious conscious intent, but Neadertals and Denisovans are creatures I think the ethical issues are strongly mitigated. After all, chimpanzees are used in medical experiments. I assume that the woolly mammoth will be the first extinct complex organism which is resurrected. But what if they’re human???

Stalin purportedly wished to create ape-human super-soldiers. What if it is true that Neandertals were, and would be, far stronger on a per unit basis than humans? Can you imagine: “unleash the Neandertal brigade!” More optimistically, what if Neandertals lacked social intelligence, but exhibited very strong aptitudes in the visuo-spatial sciences? Neandertals had average cranial capacities which were larger than modern humans.

• Category: Science • Tags: Bioethics, Neandertal, Neandertal genomics 
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23andMe finally unveiled a Neanderthal Ancestry estimation feature. I’m at ~2.4 percent. What I’m curious about is the fact that out of the 45 “friends and family” who are surveyed, only two are at 3 percent. One of my them is my sibling who I found seems to have the Neandertal copy of a dystrophin variant! I have hypothesized that this may be the reason for his relatively robust build (he looks a lot like me, except kind of Neandertaloid). Also of curiosity, I’m the least Neandertal in my family, including my parents!

• Category: Science • Tags: Anthropology, Neandertal, Personal Genomics 
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A few people have pointed me to the recent paper in Science, Tenfold Population Increase in Western Europe at the Neandertal–to–Modern Human Transition. The basic result is obvious, and not totally revolutionary: anatomically modern humans may simply have demographically absorbed the Neandertals (the word “absorbed” has many connotations here obviously). The results are clear in this figure:

This is not surprising, even though I have only a glancing familiarity with the guts of paleontology I was aware that there’s a lot of inferential evidence that Neandertals were not as efficient at extracting resources from any given piece of territory as modern humans. In The Dawn of Human Culture the paleoanthropologist Richard Klein offered a straightforward biological explanation for why and how the neo-African populations so rapidly marginalized Neandertals: some sort of macromutation which allowed for language and so the protean flexibility of human culture.

Implicitly this was the conventional wisdom until the likelihood of Neandertal admixture was discovered, and earlier the fact that Neandertals seemed to share the derived FOXP2 variant (the “language gene”). The earlier inferences of human demography using mtDNA, and later ancient DNA extractions from mtDNA, also seemed to align well with the proposition that there was a clean replacement of Neandertals across their range by modern populations (and the Y and autosomal results were supportive of this model too).

In hindsight it may be that these earlier genetic methodologies simply lacked the power to smoke out low levels of autosomal admixture on the scale of a few percent. Uniparental lineages have a tendency to fluctuate and go extinct fast, so the lack of the Neandertal lineages in modern populations may be a specific instance of a broader tendency whereby the vast majority of ancient lines of ancestry are extinguished.

So what smoking gun did the neo-Africans have which allowed them to be fruitful and multiply? The demographic assimilation by massive numbers is clear all across the world; there’s a reason that the “Out of Africa” model has found broad support in both morphology and genetics. Not only did the neo-Africans swarm over the northern and eastern landscapes dominated by other hominin lineages, but they were moving into the territory of others. This is quite the mean feat.

But today I think we need to revisit both the idea that Neandertals were qualitatively differently from us in a deep species-level sense, and that there need be one smoking gun to explain it all. That’s because I think we have many cases of more recent replacements and assimilations on the scale of that of the Neandertals. In the New World Europeans and Africans have replaced and assimilated the indigenous population in many regions which were ecologically suitable. In places like the Dominican Republic indigenous ancestry does persist at low levels, especially in the mtDNA, but it is not longer salient or culturally relevant in a concrete (as opposed to symbolic) sense. There were major biological differences between these Old World populations and the indigenous ones, mostly having to do with susceptibility to disease. Still, we can not separate biological advantages of the new populations from their cultural context. Malaria resistance amongst Africans became prevalent only with the rise of agriculture, as broad swaths of wilderness were cleared and transformed into farmland which was a superior environment for the mosquitoes which transmitted the pathogen. Similarly, the various infectious agents to which Europeans were inured spread via long distance contacts, which could exhibit a scale in Eurasia unmatched in the New World thanks to the emergence of a genuine ecumene.

The Columbian Exchange looms large in part because it is well documented and concerns Europeans, but genetic, linguistic, and archaeological data from Southeast Asia strongly implies that the ancient hunter-gatherers of both the mainland and the maritime zones have been assimilated by successive waves of agriculturalists issuing from the margins of southern China. There is also now evidence of massive population shifts in Europe and India due to the spread of agriculturalists. If an alien archaeologist examined the data I do think they might posit that were a biological speciation events which might explain this, as new traits arose which allowed the farming population to expand and replace the hunter-gatherers. Some of this is actually straightforwardly plausible. Consider the spread of lactase persistence or the ability of farming populations to digest amylose. But neither should we ignore the possibility of biobehavioral changes over time. Last year reading about the cultural history of Australian Aborigines I was struck by accounts of missionaries as to the different experiences in Polynesia, Melanesia, and Australia. In the two earlier cases the common strategy had been to convert “big men,” which immediately brought over whole populations. This simply did not yield in Australia, where missionaries had to target on a much finer-grain, as members of an individual band were just as liable to assume that their leader had gone crazy if he converted to Christianity than not. The leaders of these bands did not have the social capital to enforce group level cultural change. In contrast the populations of Polynesia and Melanesia had very different structures and organizations for thousands of years (e.g., agriculture) which were much more top-down than those of Australia. And it may be that not only did deeply embedded values differ, but the average personality profile may have shifted due to cultural selection upon the extant standing variation in the trait.

If there was a great leap forward to behavioral modernity ~40,000 years ago, then I think one should logically assert that there was another “great leap forward” ~10,000 years ago in the Middle East with the first farmers. There was also another “great leap forward” ~5,000 years ago ago with the invention of writing. There was another “great leap forward” ~300 years ago in Western Europea with the crystallization of a genuine scientific community.

I’m not actually suggesting that what happened 10,000 years ago was a speciation event. What I’m suggesting is that the near past may be more similar to the distant past than we imagine. This makes the near past more exotic, and the distant past less exotic.

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So asks a commenter below in relation to the question above. First, why would one even presume that they were red-haired, see my 2007 post, or the paper in Science: A Melanocortin 1 Receptor Allele Suggests Varying Pigmentation Among Neanderthals. In humans loss of pigmentation can usually be thought of as loss of function on genes. That’s probably one reason that there are several different genetic architectures for light skin, but only one for very dark skin. There might be only one way for an engine to operate as designed, but there are many different ways you can tweak a part and render it broken.

The reason that scientists have posited that Neanderthals were red-haired is that they examined the region around a melanocortin receptor gene which serves as something of a master regulator in terms of melanin production. Their sample was of two Neanderthals, one from Italy and one from Spain, and both exhibited signs of loss of function within this region. An N = 2 is small, but one must recall the fact that they are independent draws as they were sampled from different regions. Also, since then from what I recall in the Denisovan paper the authors noted that all four of their Neanderthals, from Spain, to Italy, to Croatia, to the Caucasus, seem to have a shared recent common history back to an extreme population bottleneck. If Neanderthals were relatively genetically homogeneous spatially, they may also have exhibited phenotypic similarities (thought perhaps not, due to the power of natural selection to reshape populations).

But back to the question about what Neanderthal looked like. I’m sure you’ve heard the old chestnut that if you made a few hygienic changes and had a Neanderthal don modern clothing no one would bat an eye. I’ve obtained an artist’s reconstruction of a red-haired Neanderthal in contemporary dress after a visit to a barber:

Image credit: Hoggarazzi Photography

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Image credit:ICHTO

Recently something popped up into my Google news feed in regards to “Neanderthal-human mating.” If you are a regular reader you know that I’m wild for this particular combination of the “wild thing.” But a quick perusal of the press release told me that this was a paper I had already reviewed when it was published online in January. I even used the results in the paper to confirm Neanderthal admixture in my own family (we’ve all been genotyped). One of my siblings is in fact a hemizygote for the Neanderthal alleles on the locus in question! I guess it shows the power of press releases upon the media. I would offer up the explanation that this just shows that the more respectable press doesn’t want to touch papers which aren’t in print, but that’s not a good explanation when they are willing to hype up stuff which is presented at conferences at even an earlier stage.

A second aspect I noted is that except for Ron Bailey at Reason all the articles which use a color headshot use a brunette reconstruction, like the one here which is from the Smithsonian. But the most recent research (dating to 2007) seems to suggest that the Neanderthals may have been highly depigmented. This shouldn’t be too surprising when one considers that they were resident in northern climes for hundreds of thousands of years.

But there are some new tidbits, from researchers in the field of study:

“There is little doubt that this haplotype is present because of mating with our ancestors and Neanderthals,” said Nick Patterson of the Broad Institute of MIT and Harvard University. Patterson did not participate in the latest research. He added, “This is a very nice result, and further analysis may help determine more details.”

David Reich, a Harvard Medical School geneticist, added, “Dr. Labuda and his colleagues were the first to identify a genetic variation in non-Africans that was likely to have come from an archaic population. This was done entirely without the Neanderthal genome sequence, but in light of the Neanderthal sequence, it is now clear that they were absolutely right!”

The modern human/Neanderthal combo likely benefitted our species, enabling it to survive in harsh, cold regions that Neanderthals previously had adapted to.

“Variability is very important for long-term survival of a species,” Labuda concluded. “Every addition to the genome can be enriching.”

Since Nick comments here on occasion I probably should have asked him what he thought of these results back in January, but it goes to show that I’m not thinking like a journalist. Yet.

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John Hawks, Europe and China have different Neandertal genes:

This is very striking. China and Europe by and large have different Neandertal-derived haplotypes. Haplotypes from Neandertals that are common in Europe — say, with more than two or three copies — are mostly rare in China. And vice-versa; haplotypes that are common in CHB are rare in CEU.

Why should this be? Green and colleagues…hypothesized an early population mixture of Africans and Neandertals in West Asia, before that population dispersed throughout the rest of Eurasia. This hypothesis was meant to explain why China and Europe have the same proportion of Neandertal genes.

I think that is also consistent with the fact that China and Europe have different Neandertal genes. If the population mixture was followed by substantial genetic drift as the West Asian population dispersed in different geographic directions, drift would randomly increase the frequency of some haplotypes in one direction, others in the other direction. Europe and China would end up with the same proportion of Neandertal ancestry, but it would be distributed very differently among loci.

Next, we’ll examine whether this pattern is the same for the rest of the chromosomes. Or maybe something even more interesting…

Guesses? I’m assuming it has something to do with adaptation.

• Category: Science • Tags: Evolution, Neandertal 
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Last week I reported that it turns out that one of my siblings carry a possible Neandertal haplotype on the dystrophin gene. To review, it seems likely that ~3% of the average non-African’s genome is derived from Neandertal populations. But by and large this ancestral quantum seems broadly dispersed through the genome of individuals, so that there isn’t a particular set of loci which are Neandertal, as such. As an analogy, about ~20-25% of the genome of an average black American is derived from Europe because of white American ancestry. But you can’t usually predict from that on which locus the “white” alleles will be found. The main exception to this will be loci where you might suspect selection will be operative, such as those implicated in malaria defense (some of them have negative consequences).

The dystrophin haplotype though has higher frequencies in some populations than expectation. ~9% in non-Africans as a whole, and higher in some groups. So there was a reasonable expectation that people might find that they carried it snooping through their genomes. Now that my parents (RF and RM) have come through, as well as sibling #2 (RS2), I can show you this:

rs1456740 rs6628685 rs331370 rs2854965 rs6653863 rs331369 rs331368 rs331367 rs331366
Razib G A C G (not typed) C T T G
RS2 A A (no call) G A A T T T

As you can see RS2 and RF have a single copy of the Neandertal haplotype. That’s because males only have one X chromosome. In contrast, females have two, so you can’t know immediately what the haplotype necessarily is just by looking at the sequence of genotypes which you can extract out of the 23andMe browser. But since males inherit the X chromosome from their mother, one can infer that my mother is a heterozygote for the Neandertal haplotype, B006, and B001, the most common Eurasian one. So here’s what I can figure out:

rs1456740 rs6628685 rs331370 rs2854965 rs6653863 rs331369 rs331368 rs331367 rs331366

Razib G A C G (not typed) C T T G
RS2 A A (no call) G A A T T T

Obviously I don’t know if there’s any functional significance which correlates with these markers. But note that on this particular locus I’m 0% Neandertal, while RS2 is 100% Neandertal, while RS1 and RM are 50% Neandertal. Though I doubt that the quantum of total Neandertal admixture differs at all within the family, there’s going to be variance at any given locus (though on most loci presumably the alleles will be descended from neo-Africans across the family).

Note: for the record, I am moderately disappointed that I didn’t win the Neandertal genetic lottery on this locus.

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After 2010’s world-shaking revolutions in our understanding of modern human origins, the admixture of Eurasian hominins with neo-Africans, I assumed there was going to be a revisionist look at results which seemed to point to mixing between different human lineages over the past decade. Dienekes links to a case in point, a new paper in Molecular Biology and Evolution, An X-linked haplotype of Neandertal origin is present among all non-African populations. The authors revisit a genetic locus where there have been earlier suggestions of hominin admixture dating back 15 years. In particular, they focus on an intronic segment spanning exon 44 of the dystrophin gene, termed dys44. Of the haplotypes in this they suggested one, B006, introgressed from a different genetic background than that of neo-Africans. The map of B006 shows the distribution of the putative “archaic” haplotype from a previous paper cited in the current one from 2003. As you can see there’s a pattern of non-African preponderance of this haplotype. So what’s dystrophin‘s deal? From Wikipedia:

Dystrophin is a rod-shaped cytoplasmic protein, and a vital part of a protein complex that connects the cytoskeleton of a muscle fiber to the surrounding extracellular matrix through the cell membrane. This complex is variously known as the costamere or the dystrophin-associated protein complex. Many muscle proteins, such as α-dystrobrevin, syncoilin, synemin, sarcoglycan, dystroglycan, and sarcospan, colocalize with dystrophin at the costamere.

Dystrophin is the longest gene known on DNA level, covering 2.4 megabases (0.08% of the human genome) at locus Xp21. However, it does not encode the longest protein known in humans. The primary transcript measures about 2,400 kilobases and takes 16 hours to transcribe; the mature mRNA measures 14.0 kilobases….

Dystrophin deficiency has been definitively established as one of the root causes of the general class of myopathies collectively referred to as muscular dystrophy. The large cytosolic protein was first identified in 1987 by Louis M. Kunkel…after the 1986 discovery of the mutated gene that causes Duchenne muscular dystrophy (DMD) ….

OK, so we’ve established that this is not an obscure gene. Here’s the abstract of the new paper:

Recent work on the Neandertal genome has raised the possibility of admixture between Neandertals and the expanding population of H. sapiens who left Africa between 80 Kya and 50 Kya to colonize the rest of the world. Here we provide evidence of a notable presence (9% overall) of a Neandertal-derived X chromosome segment among all contemporary human populations outside Africa. Our analysis of 6092 X-chromosomes from all inhabited continents supports earlier contentions that a mosaic of lineages of different time depths and different geographic provenance could have contributed to the genetic constitution of modern humans. It indicates a very early admixture between expanding African migrants and Neandertals prior to or very early on the route of the out-of-Africa expansion that led to the successful colonization of the planet.

The authors do consider the possibility that the B006 haplotype is derived from a common haplotype spanning Eurasian hominins and northeast Africans. They reject this on the grounds that the only African populations where such sharing with Eurasians occurs occurs are known to have been subject to recent back-migration (this presumably includes the Maasai). Additionally, they assert that “oldest lineages tend to be found in South rather than North-Eastern Africa.” I’m not totally sure about the context of this assertion. Oldest lineages overall? Or for this particular locus?

In any case, here’s a table from the 2003 paper:

The peculiarity of B006 is its restriction to non-Africans, and its variance. Remember that the null hypothesis presumes and “Out of Africa,” where non-African distinctiveness should be relatively shallow. The current paper illustrates the model for how the B006 haplotype slipped into the non-African genetic background. Interestingly the authors note the presence of B006 in “a remote community of isolated indigenous Australians living in Central Australia.” Naturally the big difference between now and 2003 is the ability to compare with the Neandertal draft reference genome. They note that “In the Neandertal sequence, no information is available for 28 of these sites, 36 sites represent ancestral alleles and 13 derived alleles. Importantly, three of the derived alleles (rs17243319, rs1456729 and rs11796299 in Table S2) are absent from the African chromosomes, as in the case of the derived G of rs11795471 from within B006. Moreover, all derived alleles shared with Neandertals occur at high frequencies (0.75 and more) on a background of the extended B006 haplotype (Figure 3 and Table S2) as expected in a segment of recent Neandertal origin.”

Overall this paper illustrates two trends. First, the general one whereby research groups are going to revisit loci which exhibit signatures of admixture with Neandertals and other assorted Eurasian hominins. Prior to 2010 these results were peculiarities, published, but generally not integrated into a bigger theoretical framework (by this, I mean the scientific community did not pay much attention to the authors’ attempts to integrate their research into a counter-narrative to “Out of Africa”). Second, there will be the specific focus on particular genes with an interest in ascertaining functional significance, and possible adaptation. This is hinted at in the last sentence of the discussion: “Considering such early encounter of H.sapiens with Neandertals, a question may be raised: was this encounter coincidental and without important evolutionary consequences or…did it facilitate adaptations to novel environmental conditions that actually contributed to the successful expansion of human migrants from Africa to other continents?” Indeed.

Citation: Vania Yotova, Jean-Francois Lefebvre, Claudia Moreau, Elias Gbeha, Kristine Hovhannesyan, Stephane Bourgeois, Sandra Bédarida, Luisa Azevedo, Antonio Amorim, Tamara Sarkisian, Patrice Avogbe, Nicodeme Chabi, Mamoudou Hama Dicko, Emile Sabiba Kou’ Santa Amouzou, Ambaliou Sanni, June Roberts-Thomson, Barry Boettcher, Rodney J. Scott, & Damian Labuda (2011). An X-linked haplotype of Neandertal origin is present among all non-African populations Mol Biol Evol : 10.1093/molbev/msr024

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Neandertals famously had larger cranial capacities than modern humans, and, have gone through multiple phases of de- and re-humanization. A few weeks ago there was a revision of the idea that Neandertals in France ~30,000 years ago adopted some aspects of modern human culture through diffusion. This was a support for the Neandertal “ooga-booga” thesis. In contrast last spring we were treated to the possibility that most human beings have trace but non-trivial Neandertal ancestry. This naturally made Neandertals seem a little less primitive, since we don’t like to perceive ourselves as primitive.

A new article in Current Biology supports the position for the primitive Neanderal, Brain development after birth differs between Neanderthals and modern humans:

Neanderthals had brain sizes comparable to modern humans, but their brain cases were elongated and not globular as in Homo sapiens…It has, therefore, been suggested that modern humans and Neanderthals reached large brain sizes along different evolutionary pathways…Here, we assess when during development these adult differences emerge. This is critical for understanding whether differences in the pattern of brain development might underlie potential cognitive differences between these two closely related groups. Previous comparisons of Neanderthal and modern human cranial development have shown that many morphological characteristics separating these two groups are already established at the time of birth…and that the subsequent developmental patterns of the face are similar, though not identical…Here, we show that a globularization phase seen in the neurocranial development of modern humans after birth is absent from Neanderthals.

In other words there are developmental differences between Neandertals and modern humans. They’re a little less circumspect in the text, “We find that the modern human pattern of brain development is derived compared to Neanderthals.” The implication here is that the Neandertals exhibit the ancestral pattern, in common with chimpanzees. Below is figure 1, which summarizes their results:


(link acknowledge, Dienekes)

• Category: Science • Tags: Human Evolution, Neandertal 
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I assume by now that everyone has read A Draft Sequence of the Neandertal Genome. It’s free to all, so you should. At least look at the figures. Also, if you haven’t at least skimmed the supplement, you should do that as well. It’s nearly 200 pages, and basically feels more like a collection of minimally edited papers than anything else. There’s no point in me reviewing the paper, since you can read it, and plenty of others have hit the relevant ground already.

Since there seem to be three main segments of the paper, here are a few minimal thoughts on each.

First, the draft genome. What would you have said if someone came up to you ten years ago and told you that you’d live to to see this? Svante Paabo himself admitted he didn’t think he’d see something like this in his lifetime. There was a lot of hard work that went into figuring out how to get at the genetic material, purify it, and confirm that it was actually from the samples in question and not handler contamination and such (remember that there was a problem with contamination a few years back). To a great extent the focus on the results, instead of the methods, is like critiquing a set of landscape photographs taken from a very high peak. We can’t forget the effort and energy that went into scaling the peak itself. A lot of labor input obviously went into this, but additionally we can thank the fact that we live in a technological society where progress is not only expected, but often can’t be accounted for in our projections of future possibilities. I think that’s a very hopeful thing which makes me a little less pessimistic about the possibility of the magic carpet economy.

Second, the are the comparisons between Neandertals, modern humans, and chimpanzees. As Carl Zimmer noted there are an alphabet soup of genes thrown at you in the results. It is hard to make sense of it all, though I did note that genes involved in skin function and phenotype seem to have been the subject of differential evolution between Neandertals and modern humans (i.e., SNP differences in regards to substitutions in the lineages). We already know that there are suggestive signs that Neandertals lost function on pigmentation independently from modern humans. That shouldn’t be too surprising, given that it seems that West and East Eurasians evolved light skin independently. There are some uncertainties about the timing of this, but the different genetic architecture implies that it was unlikely to have occurred immediately after the Out-of-Africa event, and in fact some of the loci imply that depigmentation may have occurred in the Holocene. Skin is famously our biggest organ, so it shouldn’t be that shocking that it is possibly a target of selection, but curious nonetheless (recall that it seems that humans evolved darker skin from a paler ancestor as we lost our fur in the tropics).

Additionally, I think the finding that Neandertals and modern humans seem to share most of the same HARs, regions of the genome where our human lineage seems to differ from other mammals in exhibiting a lot of evolutionary change, is of great interest, though not necessarily surprising. When pointing to Luke Jostins’ post on rates of encephalization, I observed that in some ways it seems like there was a very powerful and consistent lineage specific trend toward greater cranial capacity which had incredible time depth. In The Dawn of Human Culture Richard Klein puts the emphasis on the sharp break between those populations before ~50 thousand years ago, and after. This period is marked by the shift toward behavioral, as opposed to just anatomical, modernity (there were anatomically modern humans in Africa ~200 thousand years ago). Klein’s thesis is that some mutation triggered a radical biocultural change, and was responsible for the Great Leap Forward, the efflorescence of creative symbolic culture which we truly consider the sin qua non of culture. The sharing of HARs between Neandertals and pure humans, and the consistent trend toward encephalization (aside from the post-Ice Age reversal), makes me shift the priors a touch more toward inevitable continuity and away from contingency. I find much of the politics of Robert J. Sawyer’s Neanderthal Parallax series a bit heavy-handed, but his depiction of Neandertals as fundamentally intelligent creatures who differ only on the margins seems a lot more plausible to me now than it was when I first read it in the early to mid-aughts.

Third, and finally, there’s the story of admixture and sex. This is getting all the press, but of course this is the most uncertain, inferential, and speculative aspect of the paper. It’s impressive, but it should open to skepticism, especially after the Out-of-Africa totalism which was ascendant until recently. John Hawks accepts the thrust of the findings, but obviously has his own ideas as to modifications, extensions and qualifications. Dienekes Pontikos favors an alternative interpretation of the data, which the authors point to in the text but dismiss as less parsimonious. My own inclination is to favor the authors in their interpretation of parsimony, but I will admit that this assertion is disputable. Dienekes and others would suggest that it is just as, or more, plausible that the shared variants between non-Africans and Neandertals arise from their common northeast African ancestral population (or some ancestral population of non-Africans and Neandertals). He rightly points out that there may be ancient population substructure within Africa, and using a particular African group as a “reference” for the whole continent may lead to false inferences. The main issue is that the probability of retrieving ancient DNA from northeast African samples in the near future seems low because the conditions for preservation are not optimal (tropical climates famously degrade and recycle biological material more efficiently than temperate or boreal climates). Additionally, using modern northeast African populations is somewhat problematic because there has clearly been some back-migration from the nearby Arabian populations into this area in the medium-term past (the languages of the Ethiopian highlands are Semitic). One supposes that one could differentiate between the African and Arabian components of the genome of Ethiopians and Somalis, but if the admixture event was two to three thousand years ago I presume it would be technically more challenging than an African American, where very few generations have passed since admixture for recombination to fragment long genomic regions attributable to one ancestral population. In other words, how do you distinguish Neandertal variants which arrived back from Eurasia from ancient African ones? (I suppose that the haplotypes would differ so that the genuinely African ones would be more diverse)

But even if you reject the top-line finding, that most of us are not pure human, I think the paper is a game-changer in terms of shifting your priors in relation to evaluating the plausibility of a result which suggests admixture from an ancient non-African population. I found out about the high likelihood of this paper just before the UNM results were presented at the American Anthropological Society meeting, and it is clear in hindsight with the large author list that many people knew what was coming down the pipepline and had recalibrated their assessment of results which indicated admixture. It is perhaps time to go back and take a second look at papers which you skipped over before because it seemed that they may have been spurious or reporting a statistical quirk because they lay outside of the orthodox paradigm. This is clearly a case where it is good to live in interesting times.

Citation: Green, R., Krause, J., Briggs, A., Maricic, T., Stenzel, U., Kircher, M., Patterson, N., Li, H., Zhai, W., Fritz, M., Hansen, N., Durand, E., Malaspinas, A., Jensen, J., Marques-Bonet, T., Alkan, C., Prufer, K., Meyer, M., Burbano, H., Good, J., Schultz, R., Aximu-Petri, A., Butthof, A., Hober, B., Hoffner, B., Siegemund, M., Weihmann, A., Nusbaum, C., Lander, E., Russ, C., Novod, N., Affourtit, J., Egholm, M., Verna, C., Rudan, P., Brajkovic, D., Kucan, Z., Gusic, I., Doronichev, V., Golovanova, L., Lalueza-Fox, C., de la Rasilla, M., Fortea, J., Rosas, A., Schmitz, R., Johnson, P., Eichler, E., Falush, D., Birney, E., Mullikin, J., Slatkin, M., Nielsen, R., Kelso, J., Lachmann, M., Reich, D., & Paabo, S. (2010). A Draft Sequence of the Neandertal Genome Science, 328 (5979), 710-722 DOI: 10.1126/science.1188021

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In Science Ann Gibbons has a very long reported piece, Close Encounters of the Prehistoric Kind. It’s well worth reading, but behind a pay wall. If you don’t have access though, I want to spotlight one particular section:

The discovery of interbreeding in the nuclear genome surprised the team members. Neandertals did coexist with modern humans in Europe from 30,000 to 45,000 years ago, and perhaps in the Middle East as early as 80,000 years ago (see map, p. 681). But there was no sign of admixture in the complete Neandertal mitochondrial (mtDNA) genome or in earlier studies of other gene lineages…And many researchers had decided that there was no interbreeding that led to viable offspring. “We started with a very strong bias against mixture,” says co-author David Reich of Harvard Medical School in Boston. Indeed, when Pääbo first learned that the Neandertal DNA tended to be more similar to European DNA than to African DNA, he thought, “Ah, it’s probably just a statistical fluke.” When the link persisted, he thought it was a bias in the data. So the researchers used different methods in different labs to confirm the result. “I feel confident now because three different ways of analyzing the data all come to this conclusion of admixture,” says Pääbo.

The finding of interbreeding refutes the narrowest form of a long-standing model that predicts that all living humans can trace their ancestry back to a small African population that expanded and completely replaced archaic human species without any interbreeding. “It’s not a pure Out-of-Africa replacement model—2% interbreeding is not trivial,” says paleoanthropologist Chris Stringer of the Natural History Museum in London, one of the chief architects of a similar model. But it’s not wholesale mixing, either: “This isn’t like trading wives from cave to cave; the amount of admixture is tiny,” says molecular anthropologist Todd Disotell of New York University in New York City. “It’s replacement with leakage.”

The power of data to overwhelm human prejudice is sometimes very awesome. And the bias which Reich and Pääbo exhibited was not unfounded; Pääbo was involved in the sequencing of the Neandertal mtDNA, and found no evidence of admixture there. These data were strong, and I believe they should now shift our assessment of probabilities in relation to earlier papers which claimed some admixture between the population which derives from the Out-of-Africa expansion, and the Others.

In the second section it is notable that Chris Stringer has discarded replacement as not viable. He uses the term “not trivial,” which means that it’s a significant finding of note which one can’t simply ignore when generating inferences from a set of facts which one takes as axiomatic. Disotell’s attempt to minimize the finding is more a matter of rhetoric. He does not dismiss the admixture, he simply consigns it to the undefined category “tiny.” To some extent this reminds me of the neutralist vs. selectionist arguments of the 1970s, and more recently of the Out-of-Africa vs. Multi-regionalism disputes in human evolutionary origins. An argument over the meaning of words is a matter of law, an argument grounded in empirical data and quantitative estimates is an argument about science. No one holds to the extreme caricatures of any four of the models at this point; we’ve established that all these paradigms are unchaste, now we’re just haggling over price. We know that humans and the Others did the deed, we’re now mapping out the what, where, and how often.

But this is not the closing of the gate of itjihad. Dienekes presents an alternative model which may explain the data:

There is an alternative explanation. It involves the emergence of Homo sapiens and Homo neanderthalensis from a common ancestor and the subsequent admixture of Homo sapiens with populations that have branched out before this divergence. This would account for increased similarity between Eurasians and Neandertals, but without the problem of explaining how “Neandertal” ancestry is so similar in Europeans and East Asians.

What about Africans? Why do they stand further away from Neandertals? The answer is simple: low-level of admixture with archaic humans in Africa itself. It is fairly clear to me that the sapiens line whose earliest examples are in East/South Africa must have been an offshoot of an older African set of populations. We are lucky that Neandertals lived in a climate conducive to bone (or even DNA) preservation, while the African populations inhabiting the tropics left no traces of their existence.

In conclusion: I am not at all convinced that the authors have uncovered evidence of Neanderthal admixture in Eurasians; the alternative explanation is that modern humans and Neandertals were related, modern humans spread from East Africa/West Asia and as they entered deeper into Africa, they interacted with archaic human populations there.

In his magisterial post John Hawks has hinted at more wheels within wheels. From a Kate Wong story in Scientific American:

Intermixing does not surprise paleoanthropologists who have long argued on the basis of fossils that archaic humans, such as the Neandertals in Eurasia and Homo erectus in East Asia, mated with early moderns and can be counted among our ancestors—the so-called multiregional evolution theory of modern human origins. The detection of Neandertal DNA in present-day people thus comes as welcome news to these scientists. “It is important evidence for multiregional evolution,” comments Milford H. Wolpoff of the University of Michigan, the leading proponent of the theory.

The new finding shows that “gene flow across taxonomic boundaries happens,” observes geneticist Michael F. Hammer of the University of Arizona. Hammer is among the minority of geneticists who have espoused the idea of gene flow between archaic and modern populations. His own studies of the DNA of people living today have uncovered, for example, a stretch of DNA that seems to have come from encounters between moderns and H. erectus.

I assume Wolpoff is exultant. I do not personally think that this finding necessarily is going to result in a renaissance in Multi-regionalism, but Wolpoff has been the subject of a rising tide of skepticism and dismissal these past few decades. But rather than a more robust discussion between a revived Multi-regionaism and Out-of-Africa, I think these findings, and those that are likely to follow, will force us to move past simplistic typologies and accept that human evolutionary history works itself out through the principles of population genetics, and so can only roughly be modeled in words. The devil is in the parameters.

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Here’s the UCSC Genome Browser page for the Neandertal genome. Ensembl is supposed to have something up soon, but I don’t see it. Here’s the Anfo Short Read Aligner/Mapper; you can download it on that page. Page 21 of the online supplement has some configuration file code on it which might be useful. Also, make sure to check out the supplements.

• Category: Science • Tags: Anthropology, Evolution, Genetics, Genomics, Neandertal 
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I’m still digesting the papers on the Neandertals which just came out. You can find them here. If you have questions, please read the papers first. They’re open access, so free to all. There’s a lot to mull over, and I don’t know what I can add right now, but I will note:

1) There’s a lot of stuff that doesn’t have to do with admixture, but focuses on genes where Neandertals and modern humans differ. There is for example an enrichment of differences in genes which relate to skin morphology. But my friends who think that modern human uniqueness can’t be pinned down to changes in SNPs will probably feel even more validated by this paper.

2) The fact that non-Africans as a whole, including Papuans, have Neandertal admixture, presumably from interactions in the Middle East, seem close to falsifying the “two-wave” model of expansion “Out of Africa” which came to prominence in the early aughts. That is, one group of Africans went north through the Middle East, and another swept along the Indian ocean fringe and onto southeast Asia. If there were two waves then they interacted a lot because they both received the same proportion of Neandertal alleles, which makes the idea of two genetically distinct waves a bit useless.

• Category: Science • Tags: Admixture, Evolution, Genetics, Genomics, Neandertal 
Razib Khan
About Razib Khan

"I have degrees in biology and biochemistry, a passion for genetics, history, and philosophy, and shrimp is my favorite food. If you want to know more, see the links at"