(Last Update Oct 13)
This is a wonderful paper as it directly deals with the old coalescence times of human autosomal DNA and their presumed incompatibility with the Out of Africa model:
A genome-wide frequency distribution of the TMRCAs has been reported by curatingThe four scenarios considered by the authors are seen schematically in the following figure from the paper:
the literature (Garrigan and Hammer 2006) but no systematic and consistent analysis has been performed in a single genome-wide data set. We report the fi rst genomewide estimation of the TMRCAs of anatomically modern humans, and we investigate if diff erent scenarios of human evolutionary history are supported by this estimate.
The Recent out of Africa: Single Origin Population model is the simple model that has found support in the shallow coalescence times of human Y-chromosomes and mtDNA and has made the jump to popular culture. In this model, humans are a young species that underwent a bottleneck, and Eurasians are descended from a group of Africans that left the continent. This model has been criticized for its perceived inability to explain deep divergence times in autosomal DNA.
The Recent out of Africa: Multiple Archaic Populations is the model I have advocated over the years (check out the "Palaeoafrican" label of the post for my past writings on the subject). It agrees with the previous model in the recent African origin of modern Homo sapiens but it states that the African population was structured and not panmictic: divided into fairly isolated long-standing subpopulations, and that Eurasians are descended from a single one of these African subpopulations (which I have termed "Afrasians").
The existence of a structured African population makes easy work of deep divergence times, as the variants that have such deep origins are presumed to have evolved separately in different African subpopulations, and then to have found themselves in the modern gene pool after the breakdown of this structure.
The Multi-Regional: Recent Admixture model is the one advocated by those seeing Neandertal and/or Homo erectus introgression in Eurasia. Like the previous two models, it agrees on the recent African origin of modern humans, but it sees a place for long isolated pre-existing Eurasian hominids, who contributed some of their mtDNA to modern humans.
Like the previous model, deep divergence times are no problem, as two variants with deep common ancestry are presumed to stem from the separated Eurasian and African Homo. This model has found recent support by analysis of the Neandertal genome but as the authors of that study and myself have stressed, the evidence for 1-4% Neandertal introgression into Eurasians has an alternative explanation consistent with the previous (Multple Archaic Populations in Africa) model.
Finally, the Multi-Regional: Long Standing Admixture model sees no special place for Africa, except as the point of origin of human Y chromosomes and mtDNA. Humans are descended from Homo populations from around the world that have always maintained gene flow between them. This model obviously explains deep divergence times, but has a difficult time explaining the African origin of the uniparental markers, the palaeoanthropological evidence for an emergence of anatomical modernity in East Africa and the genetic evidence for a diminution of genetic variation in Eurasia with increasing distance from East Africa.
The authors seem to propose a fifth model, Ancestral Bottleneck which is noted as a bottleneck 150,000 years ago in a possibly ancestral structured population. This model doesn't get its own figure, but can be seen in the Single Origin Population model as "Potential bottleneck 150,000 years ago".
This model seems to combine elements of the first two ones: it is an essentially single origin model for extant humans, but it keeps the possibility of structure in Africa prior to the bottleneck, and pushes the breakdown of this structure before the bottleneck.
Here is what the distribution of TMRCAs for autosomal DNA, mtDNA, and Y-chromosomes:
The authors observe that really old most recent common ancestors are predicted by all four models, so they are no reason to discount the Single Origin Population model. However, it is plain that the variance of TMRCAs observed for actual human autosomal DNA is great (the black curve is "flat"). Here is what they write:
The variance of the empirical TMRCAs is larger than the variance predicted by three of the four different models of human evolution (see Figure 2 and Supplementary Table 3), and this large variance has been interpreted as the result of archaic sub-structure in Africa (Harding and McVean 2004). Indeed, the Multiple Archaic Populations' (scenario 2) shows similar variance of TMRCAs as the empirical data, but the inflated variance of the empirical TMRCA estimates can also be due to variation in mutation or recombination rate across the 40 sequence-regions (McVean et al. 2004).
In other words, the variance is great (more young and old TMRCAs than expected), either because of variation in mutation and recombination rates (i.e., different genomic regions evolve at different paces), or because of the multiple archaic populations idea. Unfortunately, the paper does not attempt to show how e.g., a variable genome-wide mutation rate might serve to flatten the TMRCA variance of the three models that fail to reproduce the data.
When we look at uniparental markers (mtDNA and Y-chromosomes), all four models predict older ancestors than observed. Here is what they write:
The models of human evolution typically predict older TMRCAs compared to the estimated 170,000 years for mtDNA (Ingman et al. 2000) and the upper estimate of 100,000 years for the Y-chromosome (Tang et al. 2002; Wilder et al. 2004; Shi et al. 2010). For mtDNA, a TMRCA of 170,000 years is within the range of values predicted by the `Multiple Archaic Populations' scenario (P(TMRCA less than 170,000) = 0.21), but the mitochondrial TMRCA estimate is diffi cult to reconcile with the remaining three scenarios (P less than 4x10-2). For the Y-chromosome, a TMRCA of 100,000 years is clearly at odds with three of the models (P less than 6x10-4), but for the `Multiple Archaic Populations' scenario with archaic African admixture, the proportion of simulated gene trees with TMRCAs younger than 100,000 years is larger than for the other three models, albeit quite small (P = 1.5x10-2).
Thus, while all four models can perhaps account for old autosomal TMRCAs (The "multiple archaics" on its own, the other three with help from variable genome-wide evolution), none of them can account for the young ages of human Y-chromsomes and mtDNA, with "multiple archaics" again coming on top, being consistent with "mitochondrial Eve", and coming closer (but not quite) to consistency with "Y-chromosome Adam".
There are ways to reconcile all four models with the uniparental markers, however. For the Multiple Archaic Populations model, they acknowledge that the Y-chromosome problem would go away if they increased the number of these populations from their current 3, while for the rest they invoke selection to account for the recency of human mtDNA and Y-chromosomes.
The effective population size tug of war
Parenthetically, it is important to note here the problem of the effective population size, as it has fueled quite a lot of sensationalistic media stories and documentaries (of the "humans were at the brink of extinction, and then a small band of them survived and went on to conquer the world" kind).
Here are some useful observations:
High effective population size => old TMRCAs
Low effective population size => young TMRCAs
Directional selection => young TMRCAs
Balancing selection => old TMRCAs
Structured population => old TMRCAs
In order to account for the recency of human Y-chromosomes and mtDNA, scientists came up with very low population sizes for our ancestors ("the endangered tribe" meme).
Unfortunately, this has the side-effect of predicting very low ages for autosomal DNA, lower than observed! To fix one problem, another one is created.
Can we have our cake and eat it too? An idea is to invoke balancing selection in autosomal DNA, i.e., the persistence of two variants at a given locus because they confer different advantages/disadvantages and an equilibrium between them exists, not allowing one or the other to reach its destiny of fixation.
Another idea is to invoke directional selection in Y-chromosomes and mtDNA. In directional selection, competing alleles are weeded out not by the winds of fortune, but by the supremacy of the successful alleles (Adam and Eve in our case) which push them to the side.
A different idea is to invoke ancient population structure. This immediately adds time to the TMRCA (since the different sub-populations became separated), and can thus explain old divergence times.
A fourth idea is to invoke "technical" things like variable mutation rate across the genome, or see problems in the standard age estimations for Adam and Eve. That way you can explain why there are more old autosomal TMRCAs than your model predicts, or why Adam and Eve are younger.
No wonder that there is no consensus among experts!
This paper certainly shows that the multiple archaic African populations model that I have advocated is a strong contender for being close to what actually happened. A priori, I think that the ecological and climatic variation in Africa -especially due to its north-south geometrical orientation-, and the long-established presence of Homo in the continent, make it unlikely that a single population of Homo survived there at the expense of all others.
In short, I think that: humans were never endangered in Africa, never dwindled to small numbers (inferred ancestral effective population sizes in the paper are 8k for Multiple Archaic Populations and 14k for Ancestral Bottleneck), and were not a single panmictic population spanning ecological niches and climate zones.
Rather, there were always separate populations in Africa, and climatic change (and more lately behavioral/subsistence change) has resulted in an ever-present process of population fusions and fissions. One of these sub-populations, living somewhere in East Africa, accumulated enough biological advantages to become extremely successful, populating Eurasia on the one hand where some admixture with archaic Eurasians may have taken place, but, also, successfully populating the rest of Africa, where it absorbed other subpopulations of Homo in the continent itself.
UPDATE (Oct 13): Some discussion of the paper and my own theories in Gene Expression, wherein Chris Stringer, a leading proponent of the "Recent out of Africa: Single Origin Population" says that:
While Gregory Cochran thinks I'm wrong:
My new book covers all this, and your recent work, but I do agree with Dienekes on the importance of deep African population substructure to the story..
Dienekes is wrong about the Neanderthal interbreeding results being explained by African population substructure, , but there are a lot of indications that there was significant substructure. A lot of this involves work that is not yet published: I look forward to seeing the details. Some of what I hear is remarkable.For myself, I'm waiting to see data on native east Africans on segments of "Neandertal" ancestry. Let's look at native groups from Somalia, Kenya, Ethiopia, Tanzania with limited Caucasoid admixture and let's see how much "Neandertal" ancestry they have. If they don't have any, then "Neandertal" genes must have a Eurasian admixture explanation. If they have too little, then it can be explained by Caucasoid admixture in more recent times. But, if they have much more "Neandertal" admixture than Caucasoid admixture can explain, then the obvious solution is African population substructure.
Mol Biol Evol (2010) doi: 10.1093/molbev/msq265
Deep divergences of human gene trees and models of human origins
Michael GB Blum and Mattias Jakobsson
Two competing hypotheses are at the forefront of the debate on modern human origins. In the first scenario, known as the recent Out-of-Africa hypothesis, modern humans arose in Africa about 100,000-200,000 years ago, and spread throughout the world by replacing the local archaic human populations. By contrast, the second hypothesis posits substantial gene flow between archaic and emerging modern humans. In the last two decades, the young time estimates – between 100,000 and 200,000 years – of the most recent common ancestors for the mitochondrion and the Y-chromosome provided evidence in favor of a recent African origin of modern humans. However, the presence of very old lineages for autosomal and X-linked genes has often been claimed to be incompatible with a simple, single origin of modern humans. Through the analysis of a public DNA sequence database, we find, similar to previous estimates, that the common ancestors of autosomal and X-linked genes are indeed very old, living, on average, respectively 1,500,000 and 1,000,000 years ago. However, contrary to previous conclusions, we find that these deep gene genealogies are consistent with the Out-of-Africa scenario provided that the ancestral effective population size was approximately 14,000 individuals. We show that an ancient bottleneck in the Middle Pleistocene, possibly arising from an ancestral structured population, can reconcile the contradictory findings from the mitochondrion on the one hand, with the autosomes and the X-chromosome on the other hand.