December 28, 2010

Is multi-regional evolution dead?

A widely-circulated interpretation of the recent work on the genome of Neandertals and the Denisova hominins is that it proves the assimilation model of human origins. First, a reminder of the main models of human evolution from Stoneking et al.:

It is said that modern humans are mostly Out-of-Africa but there has been gene flow into regional Homo sapiens populations: Neandertal-related admixture affecting Eurasians and Denisovan-related admixture affecting Melanesians.

This naive interpretation of the evidence proposes that e.g., Melanesians are about 92% derived from Out-of-Africans and 8% derived from other hominins including both Neandertals and Denisovans.

It's important to state categorically that this only an interpretation of the evidence and in no way a disproof of the multiregional theory of human evolution.

Interbreeding happened

Let's begin by considering what we know to be true: interbreeding happened between widely divergent human populations. Otherwise the pattern of differential affiliation of modern human groups to archaic hominins would be impossible to explain: all humans should have the exact same relationship to the "side-branches" of the human family tree. But, this is clearly not the case.

If interbreeding happened then...

It's important to note how important this insight is. Modern human populations are mutually interfertile, but it is generally assumed that beyond a certain point of genetic divergence interbreeding is impossible for both anatomical and genetic incompatibility reasons.

But, if we accept the possibility of interbreeding even between very divergent populations, then where do we stop? It's possible that H. sapiens himself is the product of such interbreeding.

Admixture with archaics vs. Incomplete fusion

There are two ways of viewing the evidence:
  1. Different human populations have admixed with different archaic populations during the Out-of-Africa exodus
  2. Humans are descended from multiple archaic populations and have blended together, but the fusion is incomplete
Here is the Reich et al. model:

The alternative model is that Eurasian and African Homo can be envisioned as a mosaic of populations that did not speciate because gene flow between most of them was never interrupted.

Adaptive changes could flow freely in the lattice of populations: they could originate anywhere and spread across the entire species range in a few thousands of years.
  • Part of the regional variation spread and became part of the species-wide variation
  • Part of the regional variation was lost either because of drift or because it was maladaptive
  • Part of the regional variation remained in regional populations
It is this latter part that causes regional populations to show differential affiliation with archaic hominins.

A color analogy

Imagine a canvas painted with an orange color. It is not uniformly orange, however: parts of it are more "red" than average, and parts of it are more "yellow" than average.

One interpretation for this canvas is that the painter used an orange hue to paint it, but small amounts of red and yellow pigment were added in parts of the painting (Assimilation model)

A different interpretation is that the painter used red and yellow hues to paint it, but even though he moved his brush left-right and top-bottom, shuffling pigments around, there was an excess of red pigment at the spot where his brush first hit the canvas. (Multi-regional model)

What about the reduced genetic diversity of our species?

An argument for the recent Out of Africa model is that the reduced genetic diversity of our species necessitates a small effective population size and a recent genealogical time depth.

With respect to the latter, it should be noted that the genetic divergence between modern humans and Neandertals/Denisovans is about 1/3 more than between the most divergent humans (Papuans and San in Reich et al.). Hence, the shallow genealogical time depth is true, but it is not that different from our next-of-kin.

With respect to the reduced genetic diversity, one idea is that it is the result of genetic drift following a bottleneck in a small African population. But, the data can just as well be explained by species-wide selection which culled genetic variation.

The multi-regional hypothesis proposes that the reduced genetic diversity of our species is due to a pattern of selection. The evidence is not inconsistent with this hypothesis, as the human species shows a clear pattern of morphological change in the last 200 thousand years.

Indeed, the fact that at 100 thousand years ago the "chin" makes its appearance in the Levant and China could be interpreted as an Out-of-Africa migration, but it could just as well be interpreted as natural selection producing a chin in different Homo populations, without necessarily any large-scale population movements.

Aren't Africans more genetically diverse?

Another argument for the Out-of-Africa theory is that since Africans are more genetically diverse, that is where humans originated. But, different genes tell different stories; there are loci where Africans sport the greatest variation, and there are those with genealogies better explained by a Eurasian origin. Indeed, recently a paper suggested that some Indian groups may be more genetically diverse than African agriculturalists in a particular genomic region.

But, again, greater African genetic diversity does not necessitate an African origin of mankind, and could be partially explained by a pattern of admixture between divergent populations. Back-migration from Eurasia is rarely considered as a possibility, but there are good reasons to suspect it. For example, Yorubans are genetically closer to Chinese than they are to San, and back-migration to Africa is a possible explanation for this.

The Y-chromosome phylogeny presents strong evidence for back-migration. The basal clades of the phylogeny (A and B) are African, suggesting an African origin of extant human Y-chromosomes, but within the M168 major human lineage, haplogroup DE-YAP has mixed African and Eurasian affiliations, while F-M89 is Eurasian. A Eurasian origin of M168 is a strong possibility.

Another possibility is the larger effective population size in Africa, related perhaps to the fact that until recently our species was well-adapted to an African environment and lacked the know-how to thrive in latitudes further from the equator. In a larger population there are more new mutations and fewer alleles are lost due to drift, hence such a population may appear to be more genetically diverse irrespective of whether or not it is the parental population.

Did archaics contribute at most 8%?

Melanesians emerge as the most "archaic"-admixed population under the assimilation model, having Denisovan/Neandertal-related admixture of ~8%. But, there is reason to doubt this.

First of all, consider that between Green et al. and Reich et al. we went from 1-4% archaic contribution in Eurasia to 1-8%. It only took one additional hominin to find extra archaic admixture. What will happen when we sample another one?

But, the most important thing is to understand how these admixture estimates are arrived at: they are derived from sequence shared by archaics and non-Africans but not with Africans:
  • Sequence in which Africans are polymorphic and non-Africans are monomorphic may be due to archaic admixture in Africa
  • Sequence where everyone is polymorphic may derive from anywhere, not necessarily from Africa; the same is true for sequence where everyone is polymorphic and derived with respect to chimpanzee
  • Sequence where Eurasians are polymorphic and Aficans are monomorphic and in which Neandertals are monomorphic may derive from non-Neandertal non-African archaic hominins
In short, we should take the admixture ceiling of 8% with a huge grain of salt.

Conclusion

At the beginning of 2010 I would describe myself as fairly agnostic on the issue of human origins, but leaning towards the Recent Common Origin hypothesis due to:
  1. The Y-chromosome and mtDNA phylogeny
  2. The 100ky gap between Omo 1 and Qafzeh and the 50ky gap between Qafzeh and the later anatomically modern humans from Eurasia
  3. The greater African genetic diversity, and its clinal diminution from east Africa
  4. The lack of evidence for interbreeding between humans and archaic hominins
2010 has destroyed factors 2-4:
  • Zhirendong Cave gave us a chin in China, 100ky, and hence Qafzeh could no longer be interpreted as the early-Out-of-Africa that failed. The gap between anatomical modernity in Africa and in Eurasia narrowed.
  • Xing et al. narrowed the presumed gap in genetic diversity between Africans and Eurasians, and showed that the diversity decrease cline is spurious.
  • Reich et al., Green et al., and Krause et al. showed us that interbreeding between Homo sapiens and divergent Homo populations must've taken place.
As the beginning of 2011 approaches I am much less convinced of Out-of-Africa with Assimilation. Hopefully, in the coming years both the 1000 genomes project and ancient DNA work on early Homo sapiens or even other archaic hominins will add more data to the discussion.

UPDATE:

Razib links to my post with some comments of his own. A few observations:
  • The importance of the Xing et al. paper is not so much in "disproving" the greater African genetic diversity. That conclusion cannot be reached from a single genetic region and without including African hunter-gatherers. Its importance is, however, in showing that the presumed smooth cline of decrease of genetic diversity from east Africa and across Eurasia is spurious; hence it weakens a crucial Out-of-Africa argument
  • Razib points out that recent selection tends to be regional (e.g., different genetic causes of light skin color in Europeans vs. Asians). That is true, but note that recent selection signatures in the last 10 thousand years should not be a guide to what happens in our species over 200-300 thousand years. Our ability to detect directional selection is time-limited: at its beginning it's lost in the noise, at its end, the selected allele is quasi-fixed. In a small and mobile population of Pleistocene hunter-gatherers, even one geographically as dispersed as Pleistocene Homo the entire process may take a few tens of thousands of years, depending on strength of selection. Hence, we are only detecting mostly recent signatures of selection that arose in dense and sedentary agricultural populations partly because older episodes of selection have already run their natural course.
  • The deep rooting of the Y-chromosome phylogeny in Africa is not in doubt, but the rooting of the major M168 clade, that accounts for surely over 90% of our species, and perhaps much more is in doubt. The point of the back-migration argument is not that Y-chromosomes did not originate in Africa (they did), but that African genetic diversity could be inflated by M168 back-migrants. I have yet to see a clear separation of African genetic diversity into what is indigenous and what can be accounted for by admixture. Hence, while the Xin et al. paper shows that the Eurasian cline of reduced diversity is not resilient to the addition of new populations, it is not at all clear to me that the greater genetic diversity of east Africans is not (at least in part) due to the trilateral admixed status of east Africans (natives, people from West Eurasia, and from deeper Africa).
  • Razib argues that we are unlikely to increase the archaic admixture percentage by much because there are only so many archaic hominins around. First of all, the multiregional model could be true even if we detected 0% archaic admixture, as long as fusion between different (not necessarily all) archaic populations was complete. But, also, we should remember that the genomic coverage of Pleistocene Homo is so geographically limited! Both Homo erectus soloensis and Homo erectus pekinensis are absent, as are the more recent hominins that might be directly relevant (e.g., Mungo Man, Dali, Zhiren). The same is true for Africa where recovery of ancient DNA seems extremely unlikely given present technology.
  • Razib points out that Fst distances between humans would be much higher under multiregional evolution, and that humans share a lot of common recent ancestry. First of all, genetic divergence dates for modern humans are about 400-600ky according to Reich et al. but we should remember that different genes tell different stories: there are both very old and very shallow coalescence times in the human genome, and a model of multiple archaic populations in Africa is a good fit for the data, as is an Out-of-Africa bottleneck 150ky, much earlier than previously thought. Add selection to the equation, and even greater time depths become plausible.
In short, I am not advocating either OoA with Assimilation or MRE at this point, but I would strongly argue that while Assimilation has become more plausible than Replacement after 2010, it's not the case that Assimilation has become more plausible than MRE.

The Human Evolution Wars have just begun...

17 comments:

Strat said...

I know it is a little OT, but as a Christian what is your take on Adam, Eve and Noah's family in light of the four models and the available data?

eurologist said...

In my opinion, it is virtually impossible that oral tradition/ transmission goes back farther than a few millennia, let alone 50,000 year or 1 million years.

So, no - there is no connection to something people put on paper a few thousand years ago.

BTW, I am a Christian by upbringing - but that does not mean at all that I take things written in the bible literally. he vast majority of Christians don't- for very good and well-established reasons.

sykes.1 said...

Is not part of the problem the tension between the Mayer-Dobzhansky biological species definition (able to produce viable off-spring) and the taxonomists usual practice of using only morphology and locality to define species?

Considering the recent evidence for so-called introversions, Mayer-Dobzhansky would lump a great many of the recognized hominins into a single species. In that case, much of the origins argument disappears.

PS. The Adam and Eve story seems to relate to the invention of agriculture, and the Noah story might be a dim recollection of the filling of the Black Sea.

Strat said...

"the taxonomists usual practice of using only morphology and locality to define species"

Taxonomists don't care about biological consistency, they only care about what is traditionally accepted as true, which often has contradictions and irregularities.

"The Adam and Eve story seems to relate to the invention of agriculture, and the Noah story might be a dim recollection of the filling of the Black Sea."

All of them are fairy tales that have no connection to the real world. All religions are man-made constructs. I am an atheist and I don't care about religious issues, I care about science and truth.

Dienekes said...

Religion (pro or con) is off-topic.

German Dziebel said...

"The deep rooting of the Y-chromosome phylogeny in Africa is not in doubt, but the rooting of the major M168 clade, that accounts for surely over 90% of our species, and perhaps much more is in doubt. The point of the back-migration argument is not that Y-chromosomes did not originate in Africa (they did), but that African genetic diversity could be inflated by M168 back-migrants."

I completely agree that African diversity is inflated by later demographic processes such as 1) Africa-internal admixture between originally small divergent populations; 2) extra-African admixture (such as Y-DNA E, mtDNA M1, U6, N1, X). But you can't entertain the possibility of extra-African admixture and at the same time continue to believe in the "African root." A phylogeny is only good if it creates a robust phylogeography, namely there must be a "trail" of budding haplogroups on the way out of Africa. if there's none, then we have a problem. If there's no "out-of" in the out-of-Africa there's no "Africa" either. If you think that Y-DNA hg E back-migrated into Africa, it erases the only possible trail showing how a Sub-Saharan population could colonize Asia. What we need to do is to ask ourselves could the CDEF clade contain a source for the AB clade?

Dienekes said...

What we need to do is to ask ourselves could the CDEF clade contain a source for the AB clade?

Not sure what you mean exactly, but the basal position of A and B with respect to the rest of the tree is not in doubt, as that status is arrived to by comparison with chimpanzee, and A is the least derived w.r.t. chimpanzee. So, unless some weird evolutionary reversals have taken place, A is the most basal clade in the human Y-chromosome phylogeny.

Gioiello said...

But that HG. E wasn't original of Africa I hypothesized when I was examining the Hg. E of Mr.Gabennesch, who was from Tyrol, with some relatives in Italian Alto Adige/Sud Tyrol, the more conservative region of Italy. Then that Hg.E was African was a dogma. Now not more. If Africa has only the original A and B and mt. L, but not L3, we can say that Africa was peopled again from Asia or Europe. See my hg. R, which certainly wasn't African in origin, and the most ancient R (R1) has migrated to Africa in very ancient times: see samples among the !Kung

Gioiello said...

Alfredo Trombetti, in his theory of the monogenesis of the language, hypothesized that human languages arose in Asia. It seemed absurd with the theory of the “out of Africa”. But now we can hypothesize that also the language was brought to Africa from these migrants from Asia and also the ancient languages of San with their clicks probably arose from these first migrants, if they, as Trombetti says, are linked with all the other languages. Otherwise the link of the African languages with all the other is too recent for having more than 60 thousand years.

German Dziebel said...

"the basal position of A and B with respect to the rest of the tree is not in doubt, as that status is arrived to by comparison with chimpanzee, and A is the least derived w.r.t. chimpanzee. So, unless some weird evolutionary reversals have taken place, A is the most basal clade in the human Y-chromosome phylogeny."

Chimp and human Y chromosomes are very divergent (see http://www.nature.com/nature/journal/v463/n7280/full/nature08700.html), and this fact was ascertained after the human Y-DNA tree had been built. So, using chimps as an outgroup is rather risky. A Neanderthal sequence would be better. One of the ways to check if there were any mutational hot spots (e.g., A mutating to G and back to A) is to see if phylogeny makes sense phylogeographically. If haplogroups fan out nicely out of the source area into the derived areas, then the phylogeny must be right. If A and B are indeed basal, but hg E emerged outside of Africa as part of the CDEF clade, then how are A and B attached to CDEF if there are no C and F members in Africa? There must be some intermediary steps. You can't have hg E perform two opposite "jobs": to be the first step in the evolution of non-SubSaharan diversity and a signature of a migration back into Africa.

terryt said...

"Let's begin by considering what we know to be true: interbreeding happened between widely divergent human populations".

I have long accepted that the evidence supports that idea, especially when we consider species other than just humans and extrapolate. It's just that now we have even more convincing evidence for the case specifically in humans.

"It's possible that H. sapiens himself is the product of such interbreeding".

I'm sure it is. In fact I'm sure the development of Homo habilis was (or whatever you wish to call the species around 2 million years ago).

"Adaptive changes could flow freely in the lattice of populations: they could originate anywhere and spread across the entire species range in a few thousands of years".

A friend has coined the term 'the wave theory of evolution' to explain the situation. Separate genes move through the species in a series of waves.

"Hence, the shallow genealogical time depth is true, but it is not that different from our next-of-kin".

And possibly goes back to the change from Australopithecus to Homo. That involved considerable change, and so preumably selection.

"Back-migration from Eurasia is rarely considered as a possibility, but there are good reasons to suspect it".

And I've mentioned the possibility, and the evidence for it, several times. Usually to disagreement from most.

"Both Homo erectus soloensis and Homo erectus pekinensis are absent"

And found in two of the regions that you determined where regions of genetic extremes in modern humans. The others being Europe (Neanderthals) and Africa (Homo rhodesiensis?).

PeggyMcErlane said...

Carleton Coon lives. His research must be taken into account. It is still valid; it is a different avenue to the truth of human taxonomy.

batman said...

Coon is still going, Erasmus Darwin keeps smiling, Linnè's taxas and Rudbecks spirit is still mirrored in the ponds of field-camps and campuses...

Though, a few of their descendants seem to have forgotten some basic issues - in terms of confusing the probable and the proven. One fundamental element of modern, human genetics is the question from which mammal - or mammals (sic!) - we descend from.'

So far we do NOT even know if we - as a specie - have arosen from the dust of time as a result of (genetic) mutation or (fenotypic) cross-breeding. One of the premisses they all seem to go by - in terming the human genome - is a double-guess:

1. We're the produce of an 'evouting' mutation - and not Gods finger...

To replace the good old 'miracle of God' we have been getting another one - described as some undescribable process that gradually happened within our females mitocondrias, during the "zygosis" (moulding) of the seed from an unknown male and the egg-yolk of a taxonomicly identical female. Gradual pregnancy, that is. A bit pregnant, a bit not pregnant. Than a new specie would occur. "Probably", according to J.R. Wallace.

2. The second presumtion is that this male and female would be one monkey - rather than an Ape, as Darwin Jr. described it.

Observing this modern-day practice around the human genome one may wonder how far out on the genetic limbs people are willing to climb - before the roots of our genome are adequately defined - scientifically.

Thankfully - on this excellent site some of the oommentators have adressed this issue, rising the awareness of some of the basic questions that the genetic maps still don't comprehend.

The basic problem as of today is that the Chimps are - most probably - NOT in close family with the first couple of naked, bipedal monkeys that came out of mammal mother - on one peculiar day, very long ago.

According to our fenotype we would be much more close to the Orangutangs. And - for all that we know - there could be just another mammal there as well - to produce the execptional, naked ape that got the gift of vocal distiction - and the ability to reproduce.

The recent study of the genetic of our fellow primates seem to have revealed that the orangos are much closer to our genotype than is the chimp. Then we may ponder wheter the composition of the new specie was a result of a mystic molding of the zygote or a regular cross-over by two different set of genotypes, produceing the thir one - as in 'us'.

http://www.ncbi.nlm.nih.gov/pubmed/21041630

Since most of us can't tell one haplogroup from another one can recommend a closer look at the fysiology and fysiognomy - called fenotype - of the chimp vs. the orangos. Thus this upfront study - of the ape-human interaction:

http://www.youtube.com/watch?v=sSXsu1CheWo

batman said...

If you forget to leaf please observe that voiced laugther is a feature specific to the human kind... ;-))

Wondering from which corner of biology the sense of experiencing enhanced pleasure and share this 'spiritual' joy in a social context - we have again to look amongst a limited number of primates.

AFAIK the only animals to express 'laugther' in a visible and sonic format are chimps and orangutangs - beside goats and dolphins.

Perhaps thats were we need to look to find the "missing link" - and a mammal that can mother the seed of an ape succesfully - to transform it into a proto-human.

Today that kind of analyzis can even be a matter of research, through the comparision of the engeneering nucleids we call gens. If one a able to keep the spirit of Darwin still alive - and keep an ubiased, purely analytic mind open to the wonders of nature and the mysteries still unexplored...

Errol said...

Hi, Dienekes. On Razib Khan's blog, I took a point you made in this post 'Is Mult-regional Evolution Dead' and stated it at Razib's site here:

http://blogs.discovermagazine.com/gnxp/2011/02/real-three-dimensional-pca/#comments

The point I took from you was that "Yorubans are genetically closer to Chinese than they are to San". Onur responded stating that this was not the case and gave these FST figures:

Yoruban-San: 0,0976
Yoruban-Chinese: 0,1913
San-Chinese: 0,2480

Dienekes, can you please intervene at the link I gave and clarify what you meant? Is Onur correct or what did you mean?

Dienekes said...

I was referring to Table S6.2 of "Genetic history of an archaic hominin group from Denisova Cave in Siberia" which shows that the divergence time of Yoruba/Chinese is smaller than that of Yoruba/San

http://www.nature.com/nature/journal/v468/n7327/full/nature09710.html#/supplementary-information

Dienekes said...

Note also that the Fst onur gives are probably derived using some sort of microarray (I've given Fst estimates for Sub-Saharans vs. Paleoafricans myself here: http://dienekes.blogspot.com/2010/12/human-genetic-variation-first.html), and most SNPs in these chips are ascertained on Hapmap or other such data collections. Paleoafricans are polymorphic in sites where Eurasians (and African farmers) are monomorphic, so there is an ascertainment bias.

I would say that the genetic divergence dates of the Denisova paper are the "state of the art" as they are based on full genome sequences (see also Figure 1 of the Denisova paper showing San as outgroup to other modern humans).