Thursday, 13 May 2010

The puzzle of Neanderthal admixture


Skhul V – one of the Skhul-Qafzeh hominins. Were they the middleman between Neanderthal genes and the modern human genome?

When I initially published my last post, I pooh-poohed the rumors about the reconstructed Neanderthal genome. How could modern humans have Neanderthal DNA when no such admixture appeared in previous analyses of mtDNA, dentition, and noncoding DNA? Any Neanderthal admixture would have to be less than 1%.

I then logged on to Razib Khan’s site. The news had just broken: modern humans outside Africa are 1 to 4% Neanderthal. I hurriedly rewrote my post and spent the rest of the day eating crow.

In retrospect, I now realize I had put too much faith in the existing data. I had also ignored the warning signs. The HBD community correctly decoded the silence that had fallen over Pääbo’s research team, as well as a remark made by Linda Vigilant.

Despite the crow-phagia, this is good news. It means the end to a long and bitter conflict between proponents of two models of human origins: ‘Out of Africa’ versus multiregionalism. Anthropologists may still disagree, but the room for disagreement has greatly shrunk from what it was only a week ago. We can now move on.

The winning model is a weak version of Out of Africa. Modern humans are largely descended from a series of population expansions that began around 80,000 years ago somewhere in eastern Africa and culminated c. 60,000 BP in a ‘big bang’ that would create 96-99% of the gene pool outside Africa. The remaining 1-4% came from archaic Europeans and Asians, i.e., Neanderthals in Europe and West Asia, and other hominins elsewhere (Almas in Siberia? Hobbits in southeast Asia?). This admixture seems to have occurred in two stages: an early one in the Middle East, when modern humans began spreading out of Africa, and a later one, when modern humans began to spread from Asia to Oceania (Dalton, 2010). Curiously, the admixture looks Neanderthal in both cases.

Did this admixture contribute anything useful? We still don’t know. Some academics had identified the new variant of the microcephalin gene as being probably of Neanderthal origin, but this variant is absent from the reconstructed Neanderthal genome. To date, Pääbo’s team is of the opinion that “the Neanderthal DNA does not seem to have played a great role in human evolution” (Wade, 2010).

Surprisingly, the same level of Neanderthal admixture was found in a French subject, a Chinese subject, and a Papuan subject. This seems to suggest that Neanderthal admixture happened when modern humans began spreading out of Africa, probably in southwest Asia. But why was there no further admixture in Europe, where the two populations co-existed much longer? If there had been, we would see more Neanderthal admixture in present-day Europeans, but we don’t.

There are several possible explanations:

1. Noise in the data obscures the higher level of Neanderthal admixture in present-day Europeans. The picture should become clearer once we have sequenced 100% of the Neanderthal genome, and not the current 60% (Richard Green in an interview on CBC).

2. Early modern Europeans were replaced by Middle Eastern immigrants when farming replaced hunting and gathering (Green et al., 2010).

3. In Europe, early modern humans greatly outnumbered the Neanderthals. Subsequent admixture thus had little effect (Green et al., 2010).

4. In East Asia and Oceania, ‘Neanderthal admixture’ is actually a proxy for something else. These regions had non-Neanderthal archaic populations that were probably more closely related to the Neanderthals than to modern humans. If so, ‘Neanderthal admixture’ in these regions may correspond, more or less, to admixture with other archaic humans (my idea).

5. Neanderthal genes entered modern Eurasian populations indirectly, via an intermediate Middle Eastern population that already had Neanderthal admixture (because of prolonged contact) while being fairly close to modern humans in appearance and behavior. Modern humans may thus have more readily intermixed with them but not with Neanderthals in Europe. The latter were so different in appearance and behavior that admixture would have been minimal (my idea).

I’m inclined toward the last two explanations. Explanation #4 would explain why the later admixture in Asia/Oceania seems to have been as ‘Neanderthal’ as the early admixture in the Middle East. Unfortunately, to test this explanation, we must first reconstruct the genome of archaic humans from the Asia/Oceania transition zone. This will be difficult, if not impossible, given the accelerated degradation of DNA in the tropics.

Explanation #5 is also tempting. Not long before modern humans began spreading out of Africa, the Middle East was home to a population with both modern human and Neanderthal characteristics, as attested by remains from Skhul and Qafzeh in northern Israel. These hominins first appeared in the Levant some 120,000 years ago, perhaps as part of an earlier out-of-Africa expansion into south Asia. Their technology was Mousterian and Neanderthal-like, but their anatomy was relatively modern with some archaic features (Kidder et al., 1992; Pearson, 1998). These “almost-moderns” existed on the periphery of a range centered on the African continent. Only a bit farther north were the Neanderthals of Europe and West Asia.

When the climate cooled during the Early Pleniglacial (70,000-55,000 BP), the southern limit of the Neanderthal range shifted accordingly. Neanderthals then occupied the Levant until the arrival of modern humans some 50,000 years ago (Grun & Stringer, 1991; Schwarcz et al., 1989; Valladas et al., 1987).

What happened to the Skhul-Qafzeh hominins? They probably moved farther south, perhaps to the Hejaz. Such a location would have been athwart the main line of expansion of modern humans as they spread out of Africa. Unfortunately, despite many interesting sites, there has been no dating so far of early human occupation in Saudi Arabia (Petraglia & Alsharekh, 2003).

References

Dalton, R. (2010). Neanderthals may have interbred with humans. Genetic data points to ancient liaisons between species. Naturenews, April 20.
http://www.nature.com/news/2010/100420/full/news.2010.194.html

Green, R.E., J. Krause, A.W. Briggs, T. Maricic, U. Stenzel, M. Kircher, et al. (2010). A draft sequence of the Neandertal genome, Science, 328, 710-722.
http://www.sciencemag.org/cgi/reprint/328/5979/710.pdf

Grun, R., and C.B. Stringer. (1991). Electron spin resonance dating and the evolution of modern humans, Archaeometry, 33, 153-199.

Kidder, J.H., R.L. Jantz, and F.H. Smith. (1992). Defining modern humans: A multivariate approach, in G. Bräuer and F.H. Smith (eds.) Continuity or Replacement. Controversies in Homo Sapiens Evolution, pp. 157-177, Rotterdam: A.A. Balkema.

Pearson, O.M. (1998). Postcranial Morphology and the Origin of Modern Humans, Ph.D. dissertation, State University of New York at Stony Brook, Ann Arbor: University Microfilms International.

Petraglia, M.D. and A. Alsharekh. (2003). The middle palaeolithic of Arabia: implications for modern human origins, behaviour and dispersals, Antiquity Journal, 77, 671–684.
http://repository.ksu.edu.sa/jspui/handle/123456789/5520

Schwarcz, H.P., B. Blackwell, P. Goldberg, and A.E. Marks. (1979). Uranium series dating of travertine from archaeological sites, Nahal Zin, Israel, Nature, 277, 558-560.

Valladas, H., J.L. Joron, G. Valladas, B. Arensburg, O. Bar-Yosef, A. Belfer-Cohen, P. Goldberg, H. Laville, L. Meignen, Y. Rak, E. Tchernov, A.M. Tillier, and B. Vandermeersch. (1987). Thermoluminescence dates for the Neanderthal burial site at Kebara in Israel, Nature, 330, 159-160.

Wade, N. (2010). Signs of Neanderthals mating with humans, New York Times, May 7, 2010.
http://www.nytimes.com/2010/05/07/science/07neanderthal.html (read)

19 comments:

Anonymous said...

Good afternoon,

And what do you think of Mr. Vendramini's theory:
Them and Us: how Neanderthal predation created modern humans?

It is quite interesting. Does this theory has any holes?

Best regards.

Dienekes said...

1. Noise in the data obscures the higher level of Neanderthal admixture in present-day Europeans. The picture should become clearer once we have sequenced 100% of the Neanderthal genome, and not the current 60% (Richard Green in an interview on CBC).

I am not holding my breath that this will turn out to be the case.

2. Early modern Europeans were replaced by Middle Eastern immigrants when farming replaced hunting and gathering (Green et al., 2010).

Middle Eastern immigrants would have just as much (if not more) Neandertal admixture, since that admixture (according to the authors' scenario) happened right at their home.

3. In Europe, early modern humans greatly outnumbered the Neanderthals. Subsequent admixture thus had little effect (Green et al., 2010).

The greatly outnumbered the Neandertals eventually, but there is no reason to think that they did so initially.

4. In East Asia and Oceania, ‘Neanderthal admixture’ is actually a proxy for something else. These regions had non-Neanderthal archaic populations that were probably more closely related to the Neanderthals than to modern humans. If so, ‘Neanderthal admixture’ in these regions may correspond, more or less, to admixture with other archaic humans (my idea).

There were actually other archaic humans in Africa itself, and even subdivision with anatomically modern humans. So, the observed pattern could just as easily be explained if there was structure in Africa itself, rather than if humans interbred with Neandertals and other archaics outside Africa. In fact the authors admit that this explains their data and list it as Scenario 4 in their paper.

Note also that the relationship between non-Africans and Neandertals could also be explained by gene flow from non-Africans to Neandertals. The authors reject this, but only by using a "trick" which uses the implicit assumption that prehistoric Eurasians that admixed with Neandertals had the same relationship vis a vis modern Yoruba and San as present-day Eurasians do.

The paper is interesting, but close the discussion on the existence of archaic admixture in extant Eurasians it does not.

Tod said...

Neanderthal genes entered modern Eurasian populations indirectly, via an intermediate Middle Eastern population that already had Neanderthal admixture (because of prolonged contact) while being fairly close to modern humans in appearance and behavior.

What would this intermediate Middle Eastern population population have been before Neanderthal admixture? Some kind of archaic human or a less evolved strain of modern human?


Neanderthals in Europe. The latter were so different in appearance and behavior that admixture would have been minimal

Yes but you would never guess that from looking at the reconstructions.

Ben10 said...

About the chin.
Why was the chin selected in modern humans and not neanderthal,
what is the adaptive function of the chin ?
Even today, some individuals seem to have a recessed chin, is it a neanderthal atavism ?

A note related to neoteny: somebody said adult neanderthal looked too different and would not be attractive to modern humans, but maybe their kids were, while being at he same time sexually mature to procreate with humans.

And If I may repeat an earlyer question, is it ANY neanderthal dna, coding or non coding, that constitute those 1 or 4 % in our genome ?
From Peter's response earlyer, I understood that is is mainly non coding dna, why is that ?

Andrew Oh-Willeke said...

"2. Early modern Europeans were replaced by Middle Eastern immigrants when farming replaced hunting and gathering (Green et al., 2010).

Middle Eastern immigrants would have just as much (if not more) Neandertal admixture, since that admixture (according to the authors' scenario) happened right at their home."

This doesn't follow. Neanderthal and modern human co-habitation appears to have lasted only 1,000 years in any one place. Middle Easterners would have admixed for that thousand years and then the process would have ended. early European modern humans who were a product of the initial admixture in the Middle East and were at the front of the wave of modern human expansion would have continued the admix on the boundaries of Nenderthal and modern human territory for a much longer period. But, if those "front of the wave" modern humans were mostly and completely replaced in a demic expansion of food producing societies from the Near East that had no Neaderthal contact after the first 1,000 years of OOA, then the additional European admixture would be erased.

The likelihood of this data coming from admixture with non-Neaderthals seems very low. Homo Erectus emerges from Africa ca. 1.8 mya, while Neaderthals emerge from Africa perhaps 1.3 mya. The Sahara pump separates the two populations in time by a vast amount. The likelihood of these different populations sharing the same mutations is vanishingly small. There could be Homo Erectus admixture in Asian populations, but this test, comparing Neanderthal genomes and modern human genomes wouldn't catch it. It would look like recent Asian specific evolutionary innovation in this study.

Tod said...

Maybe there was adaptive introgression but it was self limiting. The modern humans who encountered Neanderthals in Europe may have been behaviorally different beings to their ancestors who hybridized with Neanderthals/whatever. The introgressing alleles may have transformed modern humans by the time they entered Europe. So those entering Europe were more discriminating in their mate choice as a result of the cognitive advantages they had received from introgression.

Adaptive introgression may also have led to modern humans becoming so dangerous to Neanderthals (Atlatls In Action) that they were avoided which would further limit hybridization.

Or maybe living further north selected for smarts somehow.

anon-cheese said...

I'm the anonymous who posted a lot on the thread prior. I dub myself anon-cheese.

A O-W,
I think I understand and agree with your point. One note of optimism is that we should soon know, I would think, whether mideastern neolithic agriculture-bearers replaced paleolithic Euros all the way up to Ireland and Finland. So this branch of possibilities will be testable. Just a little more ancient DNA and it should all become pretty clear -- I can forsee no obstacles.

It's a question with a lot of interest in its own right. Being a Euro, I can't wait to find out if I am a "Sumerian" or "Anatolian" or whatever. I kind of hope so. It would just make it that much more interesting and fun to read about the early-neolithic mid-easterners and read their preserved texts, and look at their artifacts.

Peter Frost said...

Anon,

Vendramini argues that the Skhul-Qafzeh hominins were directly ancestral to modern humans. The current consensus is that they were a side branch.

Dienekes,

Are you making the following argument?

1. Modern Eurasians are descended from a subset of the African gene pool, probably located in eastern Africa.

2. The Neanderthals were descended from an earlier Out-of-Africa expansion, whose origins were more or less in the same subset.

3. This common origin within Africa explains the greater similarity between modern Eurasians and Neanderthals. Modern Africans encompass a more diverse gene pool and are thus more different from the Neanderthals.

Tod,

The Skhul-Qafzeh hominins were a side-branch that split off about 40,000-60,000 years before the advent of true modern humans. They were 'almost modern.' They had most of our anatomical traits but could not imagine as we do. They were less able to generate mental images of things that were totally unseen. Nor could they manipulate these images in all four dimensions of space and time. For the most part, they could only record and retrieve images of what they had already seen.

Ben10,

It may be that some adaptive alleles were transferred from Neanderthals to modern humans. To date, nothing has been found.

Andrew,

I agree. Perhaps Dienekes can explain what he meant.

Anon-cheese,

Personally, I don't believe that Middle-Eastern farmers replaced European hunter-gathereres. For one thing, it would mean that the physical traits of northern Europeans would have arisen within a very short time span. Many hunter-gatherers adopted agriculture almost at the threshold of human history.

Yes, there is a genetic discontinuity between late hunter-gatherers and early farmers, but the discontinuity is just as great between early farmers and present-day Europeans. The discontinuity is probably due to founder effects, i.e., the hunter-gatherers who adopted farming were probably relatively small groups that rapidly expanded at the expense of other, more numerous groups.

Dienekes said...

Are you making the following argument?

I am actually making two arguments, the one you mention (with the caveat that modern Africans are also descended from the same ancestral pool as Eurasians, but they have absorbed other Africanelements AFTER the Out-of-Africa exodus).

The second argument is that the authors are too quick to dismiss modern-to-Neandertal gene flow as an explanation for their findings, and they can do this only by assuming that moderns who admixed with Neandertals had the same relative position with respect to Yoruba and San as modern Eurasians do.

Peter Frost said...

Dienekes,

I agree that modern Eurasians correspond to a subset of the modern African gene pool. Modern Eurasians seem to descend from the expansion of an initially small African population. This population also expanded within Africa itself, while absorbing to a much greater degree the more archaic populations of that continent.

But does this sub-structure extend back in time to the earlier Out-of-Africa expansion that gave rise to the Neanderthals? (about 500,000- 300,000 years ago).

Watson et al. ("Mitochondrial footprints of human expansions in Africa" 1997) found that 13% of the subSaharan gene pool dates back to an earlier expansion c. 111,000 BP (possibly the one that produced the Skhul-Qafzeh hominins). But the rest of the gene pool seems to be associated with the same population expansion that gave rise to modern Eurasians.

I'm more skeptical about your second hypothesis, i.e., modern human to Neanderthal gene flow. The Neanderthal bones used for the analysis date to 38,000-44,000 BP. This time frame is really the very beginning of modern humans in Europe, so I would not expect to see much admixture from them.

Sagat said...

Dr. Frost,

I'm glad that you responded to Anon about Mr. Vendramini's theory. I just learned of this theory from a comment on your blog. While I find much of what he proposes to be unsubstantiated and a bit silly, I thought he raised a valid issue about Neanderthal reconstructions. I've noticed the trend to make Neanderthal more and more northern European in appearance, right down to their hair line and eye color. I can't help but think that this is extremely biased and not backed up by science. Is there any reason to believe that Neanderthals, after 500k years+ of divergent evolution, would look so similar to us?

What do we really know about the soft tissue appearance of Neanderthals? We apparently don't know when we lost our thick body hair so why the trend in recreating Neanderthals with less body hair than even some current humans have? Is it not reasonable to think that a group that evolved for hundreds of thousands of years in harsh northern climates may have been somewhat hairy? There isn't any hard evidence from what I've read that they were capable of sewing clothes, though I've read of some circumstantial evidence suggesting as much.

After giving some thought to the issue, I'm bothered by what I see as ideologically motivated depictions of Neanderthals as nothing more than squat Europeans. I do know that some Neanderthals had reddish hair and pale skin, but to portray Neanderthals with European coloring and hairlines seems to be taking it a bit too far. I was hoping you could elaborate on this issue.

Dienekes said...

But does this sub-structure extend back in time to the earlier Out-of-Africa expansion that gave rise to the Neanderthals? (about 500,000- 300,000 years ago).

I don't think we should speak of "this" substructure. Clearly, both mtDNA/Y chromosome studies and autosomal studies and physical anthropology suggest that Africa has a structured population today.

There are also a priori arguments for Africa having a structured population, namely its varied climate and ecology that must've allowed for the existence of different populations.

So, I see no problem in thinking that Africa may have been structured in the past. Obviously this structure gets broken occasionally. More recently it was broken by expansions of Bantu farmers that re-established gene flow across much of the continent; previously it was broken by the expansion of anatomically modern humans from their presumably East African cradle.

I'm more skeptical about your second hypothesis, i.e., modern human to Neanderthal gene flow. The Neanderthal bones used for the analysis date to 38,000-44,000 BP. This time frame is really the very beginning of modern humans in Europe, so I would not expect to see much admixture from them.

That is not really a problem, as admixture may have taken place in the Near East earlier, during the early exit of anatomically modern humans from Africa that is associated with Qafzeh c. 100kya.

That expansion gives ample time for any modern human DNA to enter the Neandertal gene pool (unless you think that European Neandertals did not experience substantial gene flow from their Levantine counterparts in ~60ky despite being ~2k miles from them geographically).

Tod said...

some Neanderthals had reddish hair and pale skin.

They had no needles and hence no clothes or footwear so they were kept alive by a coat of fur which likely was the common forest animal colour of reddish brown, dark on the head and upper body and lighter on the belly for a countershading effect. As ambush predators who lay doggo and let foraging animals walk into a trap they needed camouflage for concealment; certainly not red hair and light skin.

The digit ratio of Neanderthals. The Neanderthals had long ring fingers the submitted paper is Digit ratios predict polygyny in early apes, Ardipithecus, Neanderthals and early Modern Humans and pairbonding in Australopithecus Website of the researcher

Neanderthals probably had very dark skin where there was no fur as going by their 2D:4D they were polygynous and the most polygynous apes have dark skin even if the coat is red ORANG-OUTAN .

Vendramini's reconstruction is very close to the truth, it is the only one that shows the thrusting spear adapted morphology of their body, ie massively strong pectorals and hands.
and females went on hunts too

If you tried to reconstruct remains of wolves using domestic dogs as a model you would get the eyes (yellow and slanting) wrong; the ears (non floppy) wrong; the gait ( perfect-stepping) wrong, all kinds of mobility (vertical jump 6-8 feet, covering >45 miles day) wrong; how dangerous to children after training ( wolves are hard wired to prey on small erratically moving and vocalising animals) wrong. Comparing the brain size you would think wolves must have been as or more intelligent than dogs - wrong again.

According to Architecture of the nasal complex in Neanderthals: comparison with other hominids and phylogenetic significance "Neanderthals do indeed possess a configuration that is unique among hominids"

Yet not only do the reconstructions give Neanderthals modern human noses they go so far as to give them recognisably European noses (and other facial features).

When they dug up Piltdown man he came with a club shaped like a cricket bat.

Sagat said...

Tod,

Thanks for your response. Humans are essentially a self domesticated species and many of our physical features have come about from recent sexual selection, so your point about wolves and dogs is an interesting analogy.

I've spent a few days trying to find good discussions about Neanderthal appearance, but many are so emotionally attached to the idea that Neanderthals looked liked us to that they refuse to even entertain the idea that they didn't. I'd just like to get a good list of the current evidence that supports the idea of anthropomorphic Neanderthals. So far, I've seen such claims like they wore body paint and buried their dead as proof that they looked like us. I don't see the logic in this.

Hopefully, now that we have their genome sequenced, we can get a better picture of what Neanderthals looked like by comparing their DNA to ours. I'm looking forward to having these questions answered.

One point. Piltdown man was a hoax, so I'm not even sure why you used that as an example. Maybe you meant something else?

Peter Frost said...

Sagat,

Tod has provided an excellent answer, so I have little to add.
Reconstructions often reflect the prevailing ideological environment. In the past, Neanderthals were seen as subhuman brutes. Now, they're made to look like the white guy next door.

The truth is that we have little data on their soft tissues. They had an MC1R allele that produces reddish hair in a modern human, but we don't really know how this allele functioned in a Neanderthal.

I strongly suspect that they were as furry as bears, since they lived in sub-zero environments without tailored clothing.

Dienekes,

The Skhul-Qafzeh hominins were not directly ancestral to modern humans. They seem to have been part of an earlier range expansion of Paleoafricans, possibly associated with the L1 haplotype.

I agree that there was some intermixture between them and Neanderthals. But your argument hinges on gene flow from modern humans (Afrasians) to Neanderthals and not from Paleoafricans to Neanderthals.

Tod said...

Sorry, I was being a bit too tangential there. The point of mentioning Piltdown man was that the hoaxer who gave his creation a club shaped like a cricket bat must have had a very English sense of humour and a very low opinion of the scientific experts' ability to see the obvious.

Marcellin Boule did the first analysis of a complete Homo neanderthalensis and concluded Neanderthals were ape-like. He also immediately recognized that the jaw of Piltdown belonged to an ape rather than an ancient human.

Dienekes said...

The Skhul-Qafzeh hominins were not directly ancestral to modern humans. They seem to have been part of an earlier range expansion of Paleoafricans, possibly associated with the L1 haplotype.

We are certainly not in a position to speak whether they are directly ancestral to modern humans.

I see no reason to think that AMHs in the Levant or other AMHs in Africa were not absorbed by the dominant group within Homo sapiens. that represents the most recent expansion.

I agree that there was some intermixture between them and Neanderthals. But your argument hinges on gene flow from modern humans (Afrasians) to Neanderthals and not from Paleoafricans to Neanderthals.

That is incorrect, my argument does not require any gene flow between modern humans and Neandertals, only a breakdown of African population struture in Africa whereby modern humans admixed with archaic Africans that did not belong to the sapiens-Neandertal clade.

Tod said...

Neanderthals diverged one million years ago

Anonymous said...

tilt that skull down in the back so it sits like it would on a real spinal column and view the flat headed, giant thibk browed, huge jawed and giant nosed ape man, it's misleading to look at it tipped up like that so that it appears more like modern man. they could never be mistaken for a modern human