More statistical Palaeoafricans

More statistical evidence for a deep Palaeoafrican layer in modern Sub-Saharan Africans in the preprint by Ragsdale and Gravel (below). When I proposed that modern Africans are a mixture of Afrasians and diverse Palaeoafricans I only had two things to go on: greater African genetic diversity (produced by admixture between diverse Palaeoafricans and Afrasians), and cranioskeletal archaicity in known African specimens.

Current models of African origins have African groups tracing their ancestry to groups that split off 200-300 thousand years from the rest of mankind, as well as even more archaic Africans (such as the ones proposed in this preprint) that split off as early as 500 thousand years ago. I'm pretty sure there are multiple layers in-between yet to be discovered: counterintuitively archaic admixture is easiest to discover if it is more distant (as it's more distinctive). But, it's unimaginable that Afrasians admixed with people that split off 200 thousand years ago, 500 thousand years ago, and none in-between.

We now know that Eurasians are not pure Afrasian either: they have some admixture with archaic Eurasians. Interestingly, archaic Eurasians are the most deeply splitting branches of humans to have contributed to modern mankind. All African genetic lineages (both Palaeoafrican and Afrasian) are nested within Eurasian genetic variation, with the jury still out on whether this happened when (1) African Afrasian populations left Africa and met archaic Eurasians, or (2) Eurasian Afrasian populations left West Eurasia and met archaic Africans.


Related:

• Statistical Palaeoafricans

Models of archaic admixture and recent history from two-locus statistics 
Aaron P Ragsdale, Simon Gravel
doi: https://doi.org/10.1101/489401

We learn about population history and underlying evolutionary biology through patterns of genetic polymorphism. Many approaches to reconstruct evolutionary histories focus on a limited number of informative statistics describing distributions of allele frequencies or patterns of linkage disequilibrium. We show that many commonly used statistics are part of a broad family of two-locus moments whose expectation can be computed jointly and rapidly under a wide range of scenarios, including complex multi-population demographies with continuous migration and admixture events. A full inspection of these statistics reveals that widely used models of human history fail to predict simple patterns of linkage disequilibrium. To jointly capture the information contained in classical and novel statistics, we implemented a tractable likelihood-based inference framework for demographic history. Using this approach, we show that human evolutionary models that include archaic admixture in Africa, Asia, and Europe provide a much better description of patterns of genetic diversity across the human genome. We estimate that individuals in two African populations have 6−8% ancestry through admixture from an unidentified archaic population that diverged from the ancestors of modern humans 500 thousand years ago.

Link

Statistical Palaeoafricans

According to a new preprint by Durvasula and Sankararaman (D+S):

Using this method, we find that ~7.97±0.6% of the genetic ancestry from the West African Yoruba population traces its origin to an unidentified, archaic population

This ~8% matches well the ~9% of "West Africa A" in Yoruba of the model of Skoglund et al. Figure 3D. If "West Africa A" corresponds to the Archaic Ghost of D+S, then the Mende have the most of it at ~13%.

I have long maintained that the higher genetic diversity of extant Sub-Saharan Africans is the result of admixture between "Afrasians" (a population that spawned Eurasians and much of the ancestry of Sub-Saharans and which had "low" (Eurasian-level) of genetic diversity) and multiple layers of "Palaeoafricans". It would seem that one such layer has now been discovered.

Where did the Afrasians live? Recent developments pushed back the presence of modern humans in both North Africa and the Middle East, making both regions highly competitive as the cradle of the Afrasians. The odds for Sub-Saharan Africa have greatly diminished also by the discovery of late non-sapiens H. naledi in South Africa (which was naively postulated as a cradle based on the presence there today of genetically diverse San Bushmen, but who are not descendants of even Late Pleistocene South Africans), as well as of the archaic component in the genomes of West Africans. These discoveries pile up on top of known archaic skulls of late provenance in both Central and West Africa.

Remember though, that the archaic admixture in West Africans is "less archaic" (more closely related to H. sapiens) than the Neandertal/Denisovan ancestry which contributed to extant Eurasians. All Africans (modern or archaic) are a branch within the phylogeny of Eurasians, with Australoids (and now apparently East Asians too) having the deepest known strain of human ancestry inherited from the elusive Denisovans.

Archaic introgression in Pygmies

We must remember that detecting archaic admixture in Africa is a statistical power game where only a particular type of such introgression can be detected:

First, it needs to be from highly diverged Palaeoafrican sources so that it will look very different from plain H. sapiens DNA. Unlike Eurasia, there's no genome of an ancient Palaeoafrican one can compare against. All inference is based on African genomes having an improbable amount of heterozygosity in parts of their genome.

Second, it needs to have happened recently enough so that it will come in big chunks that can be distinguished from the plain H. sapiens background. Given enough time, recombination breaks down archaic segments into ever tinier bits. You can argue that an unusually long divergent haplotype with a deep TMRCA is archaic, but you can't argue that a single SNP is.

I have little doubt that most if not all of the supposedly "old divergences" between African populations are a mirage created by admixture between modern humans and archaic "Palaeoafricans" diverging and admixing at different time depths. The palaeoanthropological record is quite clear that modern humans were not the only game in town for most of the 200 thousand years since modern humans first appeared in the continent's northeastern corner.

A handful or two of archaic genomes from Eurasia needs an ever-more-complex web of admixtures to make sense of; Africa will need no less, and -if morphological variability persistence is any criterion- a lot more.

Genome Research Published in Advance February 17, 2016, doi: 10.1101/gr.196634.115

Model-based analyses of whole-genome data reveal a complex evolutionary history involving archaic introgression in Central African Pygmies

PingHsun Hsieh et al.

Comparisons of whole-genome sequences from ancient and contemporary samples have pointed to several instances of archaic admixture through interbreeding between the ancestors of modern non-Africans and now extinct hominids such as Neanderthals and Denisovans. One implication of these findings is that some adaptive features in contemporary humans may have entered the population via gene flow with archaic forms in Eurasia. Within Africa, fossil evidence suggests that anatomically modern humans (AMH) and various archaic forms coexisted for much of the last 200,000 yr; however, the absence of ancient DNA in Africa has limited our ability to make a direct comparison between archaic and modern human genomes. Here, we use statistical inference based on high coverage whole-genome data (greater than 60×) from contemporary African Pygmy hunter-gatherers as an alternative means to study the evolutionary history of the genus Homo. Using whole-genome simulations that consider demographic histories that include both isolation and gene flow with neighboring farming populations, our inference method rejects the hypothesis that the ancestors of AMH were genetically isolated in Africa, thus providing the first whole genome-level evidence of African archaic admixture. Our inferences also suggest a complex human evolutionary history in Africa, which involves at least a single admixture event from an unknown archaic population into the ancestors of AMH, likely within the last 30,000 yr.

Link

Genome Research Published in Advance February 17, 2016, doi: 10.1101/gr.192971.115

Whole-genome sequence analyses of Western Central African Pygmy hunter-gatherers reveal a complex demographic history and identify candidate genes under positive natural selection

PingHsun Hsieh et al.

African Pygmies practicing a mobile hunter-gatherer lifestyle are phenotypically and genetically diverged from other anatomically modern humans, and they likely experienced strong selective pressures due to their unique lifestyle in the Central African rainforest. To identify genomic targets of adaptation, we sequenced the genomes of four Biaka Pygmies from the Central African Republic and jointly analyzed these data with the genome sequences of three Baka Pygmies from Cameroon and nine Yoruba famers. To account for the complex demographic history of these populations that includes both isolation and gene flow, we fit models using the joint allele frequency spectrum and validated them using independent approaches. Our two best-fit models both suggest ancient divergence between the ancestors of the farmers and Pygmies, 90,000 or 150,000 yr ago. We also find that bidirectional asymmetric gene flow is statistically better supported than a single pulse of unidirectional gene flow from farmers to Pygmies, as previously suggested. We then applied complementary statistics to scan the genome for evidence of selective sweeps and polygenic selection. We found that conventional statistical outlier approaches were biased toward identifying candidates in regions of high mutation or low recombination rate. To avoid this bias, we assigned P-values for candidates using whole-genome simulations incorporating demography and variation in both recombination and mutation rates. We found that genes and gene sets involved in muscle development, bone synthesis, immunity, reproduction, cell signaling and development, and energy metabolism are likely to be targets of positive natural selection in Western African Pygmies or their recent ancestors.

Link

Complex demographic history of Western Central African Pygmies

bioRxiv doi: http://dx.doi.org/10.1101/022194

Whole genome sequence analyses of Western Central African Pygmy hunter-gatherers reveal a complex demographic history and identify candidate genes under positive natural selection

PingHsun Hsieh et al.

African Pygmies practicing a mobile hunter-gatherer lifestyle are phenotypically and genetically diverged from other anatomically modern humans, and they likely experienced strong selective pressures due to their unique lifestyle in the Central African rainforest. To identify genomic targets of adaptation, we sequenced the genomes of four Biaka Pygmies from the Central African Republic and jointly analyzed these data with the genome sequences of three Baka Pygmies from Cameroon and nine Yoruba famers. To account for the complex demographic history of these populations that includes both isolation and gene flow, we fit models using the joint allele frequency spectrum and validated them using independent approaches. Our two best-fit models both suggest ancient divergence between the ancestors of the farmers and Pygmies, 90,000 or 150,000 years ago. We also find that bi-directional asymmetric gene-flow is statistically better supported than a single pulse of unidirectional gene flow from farmers to Pygmies, as previously suggested. We then applied complementary statistics to scan the genome for evidence of selective sweeps and polygenic selection. We found that conventional statistical outlier approaches were biased toward identifying candidates in regions of high mutation or low recombination rate. To avoid this bias, we assigned P-values for candidates using whole-genome simulations incorporating demography and variation in both recombination and mutation rates. We found that genes and gene sets involved in muscle development, bone synthesis, immunity, reproduction, cell signaling and development, and energy metabolism are likely to be targets of positive natural selection in Western African Pygmies or their recent ancestors.

Link

KNM-LH1: a 23,000 year old human from Kenya

From the paper:

KNM-LH 1 and other Pleistocene African specimens, all of which are potentially sampling candidate populations for dispersals across and out of Africa during the Late Pleistocene (12–15, 50, 59), differ substantially not only from recent Africans but also from individuals drawn from Holocene LSA archaeological sites. KNM-LH 1 and other Pleistocene African specimens (found with MSA and LSA artifacts) are also distinct from most EUP individuals.

Things are looking good for my Afrasian-Palaeoafrican admixture hypothesis which postulates that modern Africans are a mixture of "Afrasians" (a group of humans that also spilled over into Eurasia and/or back-migrated to Africa) and various groups of very divergent "Palaeoafrican" populations. In the context of this hypothesis, greater African genetic diversity is understood not as the result of a bottleneck of epic proportions during Out-of-Africa, but rather as a result of admixture between the two groups.

PNAS doi: 10.1073/pnas.1417909112

Late Pleistocene age and archaeological context for the hominin calvaria from GvJm-22 (Lukenya Hill, Kenya)

Christian A. Tryon et al.

Kenya National Museums Lukenya Hill Hominid 1 (KNM-LH 1) is a Homo sapiens partial calvaria from site GvJm-22 at Lukenya Hill, Kenya, associated with Later Stone Age (LSA) archaeological deposits. KNM-LH 1 is securely dated to the Late Pleistocene, and samples a time and region important for understanding the origins of modern human diversity. A revised chronology based on 26 accelerator mass spectrometry radiocarbon dates on ostrich eggshells indicates an age range of 23,576–22,887 y B.P. for KNM-LH 1, confirming prior attribution to the Last Glacial Maximum. Additional dates extend the maximum age for archaeological deposits at GvJm-22 to >46,000 y B.P. (>46 kya). These dates are consistent with new analyses identifying both Middle Stone Age and LSA lithic technologies at the site, making GvJm-22 a rare eastern African record of major human behavioral shifts during the Late Pleistocene. Comparative morphometric analyses of the KNM-LH 1 cranium document the temporal and spatial complexity of early modern human morphological variability. Features of cranial shape distinguish KNM-LH 1 and other Middle and Late Pleistocene African fossils from crania of recent Africans and samples from Holocene LSA and European Upper Paleolithic sites.

Link

An excess of X-chromosomal diversity in Africans

A new study provides important new data for African-Eurasian differences in the X-to-autosomal ratio of nucleotide diversity.

In my opinion, an explanation for this phenomenon might be found in the back-migration into Africa of Eurasian males (belonging to Y-haplogroup E). If a Eurasian man has offspring with an African woman, then the autosomal diversity of his offspring will be more than his and less than hers (*). For the pairing's daughters, 1 X chromosome will be contributed by the Eurasian man and 1 from the African woman. But, for its sons, 1 X chromosome will be contributed by the African woman only. Thus, X chromosomal diversity in descendants of such a mixed population will be higher because Africans will contribute 2/3 of the X chromosomes but only 1/2 of the autosomes.

(*) It will probably not be halfway between them, because some increase in diversity will be contributed by mutations (or equivalently archaic introgressions) that occured in the Eurasian and African lineages since their separation.

AJHG doi:10.1016/j.ajhg.2014.04.011

Contrasting X-Linked and Autosomal Diversity across 14 Human Populations

Leonardo Arbiza et al.

Contrasting the genetic diversity of the human X chromosome (X) and autosomes has facilitated understanding historical differences between males and females and the influence of natural selection. Previous studies based on smaller data sets have left questions regarding how empirical patterns extend to additional populations and which forces can explain them. Here, we address these questions by analyzing the ratio of X-to-autosomal (X/A) nucleotide diversity with the complete genomes of 569 females from 14 populations. Results show that X/A diversity is similar within each continental group but notably lower in European (EUR) and East Asian (ASN) populations than in African (AFR) populations. X/A diversity increases in all populations with increasing distance from genes, highlighting the stronger impact of diversity-reducing selection on X than on the autosomes. However, relative X/A diversity (between two populations) is invariant with distance from genes, suggesting that selection does not drive the relative reduction in X/A diversity in non-Africans (0.842 ± 0.012 for EUR-to-AFR and 0.820 ± 0.032 for ASN-to-AFR comparisons). Finally, an array of models with varying population bottlenecks, expansions, and migration from the latest studies of human demographic history account for about half of the observed reduction in relative X/A diversity from the expected value of 1. They predict values between 0.91 and 0.94 for EUR-to-AFR comparisons and between 0.91 and 0.92 for ASN-to-AFR comparisons. Further reductions can be predicted by more extreme demographic events in excess of those captured by the latest studies but, in the absence of these, also by historical sex-biased demographic events or other processes.

Link

Happy New Year 2014

What's on your wish list for the new year in the world of anthropology and human genetics?

Here's my #1 item:

Any ancient African DNA.

The study of prehistoric Eurasians has revealed that modern populations are not simply descended from the people who lived in the same areas even a few thousand years ago.

The people best preserving the genetic legacy of central European Neolithic farmers can be found on the island of Sardinia; of west European hunter-gatherers in the shores of the Baltic; of Upper Paleolithic Siberians in the jungles of the Amazon; of Middle Paleolithic Siberians in Papua and Australia. 

And yet, the model for Africa largely remains one of continuity across two hundred thousand years, since the emergence of anatomically modern humans in eastern Africa.

There have been hints that this isn't the case; the study of modern populations has revealed evidence for both archaic African, and -more recently and surprisingly- even a little archaic Eurasian ancestry in virtually all Sub-Saharan Africans. Populations from one of the presumed cradles of H. sapiens (Eastern Africa) are now conclusively known to be recent mixtures of West Eurasians, and even the Bushmen of southern Africa, the subject of so many TV documentaries as an exemplum of the ur-Humans did not escape this admixture.

Paleoanthropology also hints that some of the people who lived in sub-Saharan Africa well into the Lower Stone Age may have been quite divergent, and so do modern human Y-chromosomes. T

So the €1,000,000 question is: who lived in Africa 5 or 10 or 50 or 100 thousand years ago?

Nuclear sequences of mitochondrial origin and gene flow in Pleistocene Africa

I haven't read this, but the idea of looking at looking at nuclear sequences of mitochondrial origin (numt) as a way of testing for archaic admixture seems interesting to me. Human mtDNA has a relatively shallow coalescence (less than 200 thousand years), with Neandertal mtDNA being a clear outgroup, and Denisovan mtDNA being an even more remote outgroup. If modern humans admixed with archaic ones (having mtDNA lineages much more remote than "Eve"), then the evidence may have been lost (due to drift) in mtDNA, but may have been preserved in the autosomes.

Anthropologischer Anzeiger, Volume 70, Number 2, July 2013 , pp. 221-227(7)

Hominin evolution and gene flow in the Pleistocene Africa

Ovchinnikov, Igor V.

Africa demonstrates a complex process of the hominin evolution with a series of adaptive radiations during several millions of years that led to diverse morphological forms. Recently, Hammer et al. (2011) and Harvati et al. (2011) provided integrated morphological and genetic evidence of interbreeding between modern humans and unknown archaic hominins in Africa as recently as 35,000 years ago. However, a genetic evidence of hybridization between hominin lineages during the Lower and Middle Pleistocene epochs is unknown and the direct retrieval of DNA from extinct lineages of African hominins remains elusive. The availability of both nuclear and mitochondrial genome sequences from modern humans, Neanderthals, and Denisovans allows collecting nuclear DNA sequences of mitochondrial origin (numts) inserted into the nuclear genome of the ancestral hominin lineages and drawing conclusions about the hominin evolution in the remote past. The mtDNA and numt analysis uncovered a deep division of mtDNA lineages that existed in African hominins in the Middle Pleistocene. The first cluster included the human and Neanderthal-like mtDNA sequences while the second consisted of DNA sequences that are known today as mtAncestor-1, a nuclear fossil of the mtDNA, and the Denisova mtDNA isolated from a bone and a tooth found in southern Siberia. The two groups initially diverged 610,000-1,110,000 years ago. Approximately 220,000 years after the primary split, the Denisova - mtAncestor-1 mtDNA lineages mixed with the mtDNA pool of an ancestral population of Neanderthals and modern humans. This admixture after the profound division is demonstrated by the transposition of the Denisova-like mtDNA sequence into the nuclear genome of an ancestor of Neanderthals and modern humans. This finding suggests the matrilineal genetic structure among the Middle Pleistocene hominins as well as the existence of gene flow between African hominin lineages. Through paleogenomic analyses, it is impossible to exclude the theory that population structure and gene flow in African hominins influenced the admixture pattern observed in the nuclear genomes of non-Africans.

Link

Criticism of Y-chromosome Adam old age

... has just appeared on the arXiv. This refers to the paper by Mendez et al. announcing the basal clade A00 of the phylogeny and estimating a TMRCA for Y-chromosome Adam of 237-581ka.

The author argues that such an old age is inconsistent with neutral theory, although that assumes no population structure in the origin of modern humans; it may very well be that A00 introgressed into the modern human gene pool via an admixture event from a different African population.

The best evidence for the authors' of the original paper choice of mutation rate is their estimate that the common ancestor of all Eurasians being ~63ky vs. ~39ky using the faster rate. While a date between these two can be probably accommodated, the ~39ky age seems difficult to accept, given that Homo sapiens had arrived in various parts of Eurasia by the mid-40ky's and had been admixing with Neandertals 47-65ky BP; a higher date would also be more in line with age estimates of Eurasian mtDNA macro-haplogroups M and N.

In any case, it's probably a good idea to get a better handle on the mutation rate: Mendez et al. rely on the autosomal rate, adjusting for the Y-chromosome; while the faster rate derives from a single Chinese deep pedigree study.

arXiv:1304.6098 [q-bio.PE]

Timing of ancient human Y lineage depends on the mutation rate: A comment on Mendez et al

Melissa A. Wilson Sayres (Submitted on 22 Apr 2013)

Mendez et al. recently report the identification of a Y chromosome lineage from an African American that is an outgroup to all other known Y haplotypes, and report a time to most recent common ancestor, TMRCA, for human Y lineages that is substantially longer than any previous estimate. The identification of a novel Y haplotype is always exciting, and this haplotype, in particular, is unique in its basal position on the Y haplotype tree. However, at 338 (237-581) thousand years ago, kya, the extremely ancient TMRCA reported by Mendez et al. is inconsistent with the known human fossil record (which estimate the age of anatomically modern humans at 195 +- 5 kya), with estimates from mtDNA (176.6 +- 11.3 kya, and 204.9 (116.8-295.7) kya) and with population genetic theory. The inflated TMRCA can quite easily be attributed to the extremely low Y chromosome mutation rate used by the authors.

Link

Haplotype that looks Neandertal-introgressed may reflect African population structure (Gokcumen et al. 2013)

From the paper:

Several scenarios can be envisioned to explain the unusual genetic variation observed at the NE1 locus: (1) recent Neandertal admixture exclusively with Eurasian populations, (2) back migration to Africa from Eurasia after Neandertal admixture with Eurasian populations, and (3) ancient African substructure maintained since before Human-Neandertal divergence (Figure 3A). 
...
The presence of African NE1 haplotypes does not support the first scenario of exclusive Neandertal admixture with Eurasian populations. Recent reports have suggested that Neandertals and Denisovans contributed their genetic material to present-day Eurasian populations and Melanesians, respectively [20], [21]. However, the variation that we observe at the NE1 locus is not consistent with direct archaic hominin admixture as discussed in these publications. We did not consider Neandertal admixture into ancient African populations because of paleoanthropological studies that only report interactions between Neandertals and modern humans outside of Africa [37].

Thinking about the last sentence, paleoanthropological studies only report interactions between Neandertals and modern humans in "parts of outside Africa", but the signal of Neandertal admixture exists all over "outside Africa". It is not incoceivable that Neandertal-admixed Eurasians back-migrated into Africa and introduced NE1 to African populations. Such hypothetical back-migrants would not appear Neandertaloid in tha paleoanthropological sense. The authors consider this possibility:

The second scenario assumes back migration into Africa from Eurasian populations after the admixture of Neandertal with Eurasian populations [38]. If such admixture occurred, the African NE1 haplotypes should represent a subset of Eurasian NE1 haplotypes. To test this, we again analyzed the phase 1 data of the 1000 Genomes Project, which includes 338 haplotypes from three African populations. Using this dataset, we found that variation within African NE1 haplotypes is significantly higher than variation within Asian and European NE1 haplotypes (p less than 10-15, Figure 3C, Figure S5). This result indicates that African NE1 haplotypes have a longer coalescence and, as such, the presence of the NE1 haplogroup among modern Africans cannot be explained by simple back migration and admixture of Eurasian haplotypes to African populations.

But, it is possible that the higher variation within African NE1 haplotypes may reflect introgression of short "Palaeoafrican" variants within the African NE1 haplotypes. Such variants would appear as excess variation, but would not be "provable" as introgression in the absence of a comparative archaic African genome. This is a recurring theme, that (part of?) the African-Eurasian diversity differential can be explained both in terms of loss of diversity in an Out-of-Africa bottleneck and a gain-of-diversity in In-Africa admixture events between divergent populations that must have lived in the large and ecologically diverse continent. Which brings us to scenario #3:

The third scenario represents the persistence of an old African substructure at the NE1 locus before the Human-Neandertal divergence (Figure 3A). This scenario explains the presence of NE1 haplotypes (that are similar to the Neandertal haplotype) among modern human populations as well as the deep, distinct lineages observed among African NE1 haplotypes. To corroborate this conclusion, we estimated the coalescence of NE1 haplotypes through network analysis (Figure S6) and found a coalescence time of between ~437 K and ~993 K years before present (YBP) for African NE1 haplotypes and ~134 K YBP and ~304 K YBP for European NE1 haplotypes. These observations collectively suggest that the most parsimonious explanation for the observed variation at the NE1 locus is that the NE1/nonNE1 haplogroups arose after the human-chimpanzee common ancestor, but before the Human-Neandertal split in Africa. As such, the variation at the NE1 locus has persisted within ancient African substructure and later spread to non-African populations.

  PLoS Genet 9(4): e1003404. doi:10.1371/journal.pgen.1003404

Balancing Selection on a Regulatory Region Exhibiting Ancient Variation That Predates Human–Neandertal Divergence

Omer Gokcumen et al.

Ancient population structure shaping contemporary genetic variation has been recently appreciated and has important implications regarding our understanding of the structure of modern human genomes. We identified a ~36-kb DNA segment in the human genome that displays an ancient substructure. The variation at this locus exists primarily as two highly divergent haplogroups. One of these haplogroups (the NE1 haplogroup) aligns with the Neandertal haplotype and contains a 4.6-kb deletion polymorphism in perfect linkage disequilibrium with 12 single nucleotide polymorphisms (SNPs) across diverse populations. The other haplogroup, which does not contain the 4.6-kb deletion, aligns with the chimpanzee haplotype and is likely ancestral. Africans have higher overall pairwise differences with the Neandertal haplotype than Eurasians do for this NE1 locus (p less than 10-15). Moreover, the nucleotide diversity at this locus is higher in Eurasians than in Africans. These results mimic signatures of recent Neandertal admixture contributing to this locus. However, an in-depth assessment of the variation in this region across multiple populations reveals that African NE1 haplotypes, albeit rare, harbor more sequence variation than NE1 haplotypes found in Europeans, indicating an ancient African origin of this haplogroup and refuting recent Neandertal admixture. Population genetic analyses of the SNPs within each of these haplogroups, along with genome-wide comparisons revealed significant FST (p = 0.00003) and positive Tajima's D (p = 0.00285) statistics, pointing to non-neutral evolution of this locus. The NE1 locus harbors no protein-coding genes, but contains transcribed sequences as well as sequences with putative regulatory function based on bioinformatic predictions and in vitro experiments. We postulate that the variation observed at this locus predates Human–Neandertal divergence and is evolving under balancing selection, especially among European populations.

Link

Admixture in Southern Africa (Petersen et al. 2013)

Related:

• The genetic prehistory of southern Africa 
• Genomic Variation in Seven Khoe-San Groups Reveals Adaptation and Complex African History

PLoS Genet 9(3): e1003309. doi:10.1371/journal.pgen.1003309

Complex Patterns of Genomic Admixture within Southern Africa

Desiree C. Petersen et al.

Within-population genetic diversity is greatest within Africa, while between-population genetic diversity is directly proportional to geographic distance. The most divergent contemporary human populations include the click-speaking forager peoples of southern Africa, broadly defined as Khoesan. Both intra- (Bantu expansion) and inter-continental migration (European-driven colonization) have resulted in complex patterns of admixture between ancient geographically isolated Khoesan and more recently diverged populations. Using gender-specific analysis and almost 1 million autosomal markers, we determine the significance of estimated ancestral contributions that have shaped five contemporary southern African populations in a cohort of 103 individuals. Limited by lack of available data for homogenous Khoesan representation, we identify the Ju/'hoan (n = 19) as a distinct early diverging human lineage with little to no significant non-Khoesan contribution. In contrast to the Ju/'hoan, we identify ancient signatures of Khoesan and Bantu unions resulting in significant Khoesan- and Bantu-derived contributions to the Southern Bantu amaXhosa (n = 15) and Khoesan !Xun (n = 14), respectively. Our data further suggests that contemporary !Xun represent distinct Khoesan prehistories. Khoesan assimilation with European settlement at the most southern tip of Africa resulted in significant ancestral Khoesan contributions to the Coloured (n = 25) and Baster (n = 30) populations. The latter populations were further impacted by 170 years of East Indian slave trade and intra-continental migrations resulting in a complex pattern of genetic variation (admixture). The populations of southern Africa provide a unique opportunity to investigate the genomic variability from some of the oldest human lineages to the implications of complex admixture patterns including ancient and recently diverged human lineages.

Link

Extremely old (237–581 kya) root of human Y-chromosome phylogeny

I had mentioned this research before, and now it has officially been published. There are three things to be excited about this new paper:

First, it forces us to consider the possibility of either (i) archaic admixture in Africa, or (ii) a much more ancient time depth of modern humans than the first fossils from Ethiopia dated to about ~200 thousand years ago.

Second, it underscores the importance of collaboration between academia and regular folk, since it was the combined contributions of academics, genetic genealogists, and the owners of the new A00 basal Y-chromosomes that made this new discovery possible.

And, third, it shows that the extraordinary can be discovered without contacting isolated tribes or seeking human bones in remote regions, but rather through careful scrutiny of large volumes of data for the proverbial needle in the haystack.

The paper developed a model of Y-chromosome mutation based on the estimate of Kong et al. Significantly, though:

If we were to use the higher mutation rate (1.0x10^-9 per base per year6) rather than a realistic range derived from whole-genome sequencing (4.39x10^-9  -   7.07x10^- 9), the estimated TMRCA for the tree incorporating A00 as the basal lineage would be 209 kya, which is only slightly older than current estimates of the TMRCA of mtDNA and the age of the oldest AMH fossil remains. We note, however, that the higher mutation rate produces an estimate for the common ancestor of all non-African Y chromosome haplogroups (C through T) of ~39 kya6 (i.e., versus ~63 kya for the mutation rate used here).

A 39kya common ancestor for Eurasian Y-chromosomes makes no sense, since we now know for sure that by that time, the differentiation of Eurasians was already well on its way and modern humans in remote parts of the Old World have been documented much earlier than that time.

A ~63kya common ancestor, on the other hand, fits nicely with my "two deserts" theory of modern human origins, according to which the ancestors of Eurasians faced an ecological crisis in Arabia when it became much drier post-70kya; that seems like a most opportune time for the major Eurasian bottleneck and the corresponding coalescence of Eurasian Y-chromosomes to a single man. And, while there is no a priori reason for Y chromosomes and mtDNA to behave similarly, the age of the "older" Eurasian ur-mother, haplogroup N at 59 thousand years, with presumably an older ancestor within mtDNA haplogroup L3 founding the Eurasian population.

Also, if modern human-Neandertal admixture had occurred  "most likely 47,000–65,000 years ago", then the expansion of modern Proto-Eurasians within a 70-60kya timeframe north Out-of-Arabia would have brought them in contact with their northern Neandertal neighbors. On the other hand, it would be incredible if modern humans experienced admixture with Neandertals but were still much later a very small population (to allow for the coalescence of their Y-chromosomes to one man ~39kya).


So, in summary, the mutation rate used by the authors seems consistent with what we know about an important calibration point of the human story.

But, who were the people in Africa responsible for the introgression of A00 chromosomes? Mendez et al. used the haplotype of the African American A00 individual and discovered his patrilineal kin among the Mbo of Cameroon, who are Bantu farmers. 

I have observed before that Pygmies and Bushmen represent only a tiny fraction of pre-existing African genetic diversity, the part that had not yet been absorbed into the farmers' expanding population by the time that Africa came to the attention of of modern science. We see traces of Pygmy and Bushman ancestry in some African farmers, and there were probably other groups, no longer extant as distinct ethno-cultural entities, but, nonetheless, surviving as genetic fragments in the genomes of the farmers.

Thus, while it still makes sense to study the surviving hunter-gatherers of Africa who make up perhaps a percent or less of the population of Africa, it may be equally important to study different groups of African farmers who may possess a much richer treasure trove (albeit diluted) of such "Palaeoafrican" ancestry.

Finally:

Although the stochastic nature of the evolutionary process can explain the aforementioned incongruences, the extreme age and rarity of the A00 lineage point to the possibility of a highly structured ancestral population, consistent with recent work on the autosomes.40,41,43,44 This could take the form of long-standing population structure among AMH populations45 or archaic introgression from an archaic form into the ancestors of AMHs.46 Interestingly, the Mbo live less than 800 km away from a Nigerian site known as Iwo Eleru, where human skeletal remains with both archaic and modern features were found and dated to ~13 kya.47 Further surveys in sub- Saharan Africa and in the African Diaspora might uncover more diverged basal lineages, which will help to disentangle some of the complex evolutionary processes that shape patterns of Y chromosome diversity.

AJHG 10.1016/j.ajhg.2013.02.002

An African American Paternal Lineage Adds an Extremely Ancient Root to the Human Y Chromosome Phylogenetic Tree 

Fernando L. Mendez et al.

We report the discovery of an African American Y chromosome that carries the ancestral state of all SNPs that defined the basal portion of the Y chromosome phylogenetic tree. We sequenced ∼240 kb of this chromosome to identify private, derived mutations on this lineage, which we named A00. We then estimated the time to the most recent common ancestor (TMRCA) for the Y tree as 338 thousand years ago (kya) (95% confidence interval = 237–581 kya). Remarkably, this exceeds current estimates of the mtDNA TMRCA, as well as those of the age of the oldest anatomically modern human fossils. The extremely ancient age combined with the rarity of the A00 lineage, which we also find at very low frequency in central Africa, point to the importance of considering more complex models for the origin of Y chromosome diversity. These models include ancient population structure and the possibility of archaic introgression of Y chromosomes into anatomically modern humans. The A00 lineage was discovered in a large database of consumer samples of African Americans and has not been identified in traditional hunter-gatherer populations from sub-Saharan Africa. This underscores how the stochastic nature of the genealogical process can affect inference from a single locus and warrants caution during the interpretation of the geographic location of divergent branches of the Y chromosome phylogenetic tree for the elucidation of human origins.

Link

Deep mtDNA substructure in southern Africa (Barbieri et al. 2013)

The Khoisan have been used in many different ways in reconstructions of human history.

Being probably the most genetically diverse modern human population, they are occasionally viewed as akin to the ur-humans, with everyone else shedding diversity via founder effects as they moved away from a south African modern human urheimat.

They are also sometimes viewed as a basal branch of the human family tree, and they probably are -if modern humans are made to fit a tree model. But, modern humans didn't really evolve tree-like (some African farmers have Khoisan-like admixture, and the Khoisan themselves have relatively "shallow" common ancestry with other Africans and many Eurasians on account of their possession of a respectable frequency of Y-haplogroup E).

I have sometimes noted that in the case of South African groups were are lucky that the Khoisan exist as a discrete set of populations, making it easier to discern the legacy of South African hunter-gatherers in the genomes of immigrant farmers and pastoralists who converged southwards over the last few thousand years. This can be contrasted with the presumable situation in places like West Africa (the cradle of Sub-Saharan African farming), in which any indigenous hunter-gatherer groups have ceased to exist as distinct entities a long time ago.

A new AJHG paper sample south African genomes extensively and arrives at a startling conclusion. In the words of the authors:

Overall, the results of this analysis indicate that it is very unlikely that the highly divergent L0k1b/L0k2 lineages were incorporated into the Bantu-speaking populations via gene flow from a population that was ancestral to a Khoisan population in our sample but subsequently lost from the Khoisan population via drift. Instead, these results support the hypothesis that the ancestors of the Bantu-speaking populations carrying the divergent L0k lineages (who now live mainly in Zambia) experienced gene flow from a pre-Bantu population that is nowadays extinct. Alternatively, it is possible that descendants from this pre-Bantu population do exist but have not yet been included in population genetic studies; however, our extensive sampling of populations from Botswana, Namibia, andWest Zambia (which includes representatives of nearly all known Khoisan groups) makes it highly unlikely that this pre-Bantu Khoisan population has not yet been sampled.

In other words, we must resist the tendency to think of the Khoisan as representatives of all pre-Bantu south Africans. The Khoisan are certainly descendants of old south Africans, and represent a part of the pre-Bantu genetic landscape that retained its cultural distinctiveness (and hence can be nowadays sampled as a distinct population). But, there were other, now submerged, peaks in that landscape that are no longer extant in distinct form, but only in absorbed form in the gene pool of south African farmers.

This is fairly interesting in itself, and certainly ought to change our belief about what Africa looked like pre-Bantu expansion. We ought to think of, perhaps, a cornucopia of groups: many of them may have gone extinct; some may have been completely absorbed into more successful ones, and perhaps only a handful survive as distinct entities. Such a view would agree with the conclusions of physical anthropology about the persistence of archaic-leaning groups in parts of Africa down to the Holocene boundary.

The American Journal of Human Genetics, 17 January 2013 doi:10.1016/j.ajhg.2012.12.010

Ancient Substructure in Early mtDNA Lineages of Southern Africa

Chiara Barbieri et al.


Among the deepest-rooting clades in the human mitochondrial DNA (mtDNA) phylogeny are the haplogroups defined as L0d and L0k, which are found primarily in southern Africa. These lineages are typically present at high frequency in the so-called Khoisan populations of hunter-gatherers and herders who speak non-Bantu languages, and the early divergence of these lineages led to the hypothesis of ancient genetic substructure in Africa. Here we update the phylogeny of the basal haplogroups L0d and L0k with 500 full mtDNA genome sequences from 45 southern African Khoisan and Bantu-speaking populations. We find previously unreported subhaplogroups and greatly extend the amount of variation and time-depth of most of the known subhaplogroups. Our major finding is the definition of two ancient sublineages of L0k (L0k1b and L0k2) that are present almost exclusively in Bantu-speaking populations from Zambia; the presence of such relic haplogroups in Bantu speakers is most probably due to contact with ancestral pre-Bantu populations that harbored different lineages than those found in extant Khoisan. We suggest that although these populations went extinct after the immigration of the Bantu-speaking populations, some traces of their haplogroup composition survived through incorporation into the gene pool of the immigrants. Our findings thus provide evidence for deep genetic substructure in southern Africa prior to the Bantu expansion that is not represented in extant Khoisan populations.


Link

A00 at FTDNA2012: history in the making?

I've been following the #FTDNA2012 tag on twitter where Dr. Mike Hammer has been  talking about A00, the new most basal clade of the human Y-chromosome phylogeny. Apparently, 338ky old Y-chromosome ancestor for modern humans, at 98% confidence, with most basal clade found in western Cameroon and in African Americans separated by ~500 years from Cameroonian chromosome.

Root of human Y-chromosome phylogeny is now much older than both mtDNA Eve and first modern human fossils.

Conference attendees feel free to correct/supplement my understanding of what was said.

UPDATE: With respect to the confidence interval, Bonnie Schrack says:

The 338,000 years ago figure was the median (middle) of the confidence interval, which I believe was 95%, and not 98%. The lower limit of the confidence interval was still a bit over 200,000, I think -- that is, still before the time when fossils have been found showing fully anatomically modern features. Mike specifically said that even if the true age of A00 varied by 10 or 20% from the estimate, it would still be before the time when anatomically modern humans are thought to have appeared. I don't remember the upper limit too clearly, but as I recall, it was over 500,000 ybp.

UPDATE II: There is some uncertainty about the level of significance, with different people remembering anything from 90-98%. Some newer information from Tim Janzen:

Michael gave a TMRCA estimate of 338,000 years with a confidence interval range of 246,000 and 563,000 years for the A00/A0 node. He gave a TMRCA estimate of 202,000 years with a confidence interval range of 133,000 to 366,000 years for the A0/R-M269 node.

I guess we will have to wait for the publication to see the exact numbers, but it certainly appears that A00 branched off from the rest of mankind at an age that is much earlier than the next most basal clade (A0).

D-statistics reveal contrast between Yoruba and San in "Neandertal ancestry"

I have been exploring the HGDP version released by Patterson et al. (2012) in order to see whether patterns  of "archaic Eurasian" admixture could be detected in living Africans. In a previous experiment, I looked into a surprising link between Denisovans and Africans. Now, I want to investigate possible differences in Neandertal ancestry within Africa itself. An ASHG 2012 abstract suggests that both Neandertal and Denisovan ancestry may be relevant to the African story.

Previous research has concluded that living African groups do not appear to have substantial differences in their apportionment of archaic Eurasian ancestry. This has led to the reasonable idea that the signal of Neandertal admixture in non-Africans was driven by the encounter of Out-of-Africans with a Neandertal population in Asia, perhaps in the Near East, during their early steps outside Africa, involving a single or limited episodes of admixture, although more complex models may be needed as of late.

I have long suspected that part of this signal is due to population structure in Africa itself, and the possibility of archaic admixture in that continent, a hypothesis that is feasible a priori due to the geographical and ecological diversity of Africa and its large surface area, and which has also found support on the basis of recent palaeoanthropological and genetic research. In my opinion, the well-known abundance of polymorphism in Africans vis a vis non-Africans is not only due to the Out-of-Africa bottleneck, but may also be due to an addition of polymorphism via admixture with divergent native African hominin groups.

Advancing a good case for this admixture is rendered difficult by two factors:

1. The inability of methods relying on linkage disequilibrium to operate on old admixture events, due to the exponential decay of LD over time, which renders archaic-introgressed segments pitifully small at long time scales.
2. The high temperatures prevalent in sub-Saharan Africa which render DNA preservation problematic, although, to be honest, I have not even seen many attempts to test this hypothesis on whatever prehistoric skeletal remains there do exist from the region.

Why do African groups appear so little different in terms of possible "Neandertal admixture"? I conjecture that the answer lies in the idea that archaic African admixture will tend to even out the signal of Neandertal admixture. To use a geographical analogy, there is little distance difference (in relative terms) between Tokyo and Beijing from the vantage point of New York, but quite a lot from the vantage point or Hong Kong. Tests of archaic admixture rely on relative allele sharing between individuals or populations; consequently, the signal may be muddied by the occurrence of archaic admixture in Africans which -to use our geographical analogy- transposes them from Hong Kong to New York.

Now, consider the Z scores of the D-statistic of the form D(African1, African2, Neander, Outgroup) calculated using different panels and Outgroup being Chimp, Gorilla, or Orang. The raw numbers can be found in this spreadsheet.

Look at the Pearson correlations between the different panels:

While the Z-scores in most of the panels are strongly correlated with each other, the San panel #4 is strongly anti-correlated. An inspection of the raw numbers show why this is the case. For example:

Surprisingly, the San appear more Neandertal-admixed than the Yoruba using all Eurasian and the Yoruba ascertainment, and less so, using the San ascertainment!

A possible explanation for this pattern involves Eurasian back-migration into Africa combined with differential archaic African admixture.

The San may possess Eurasian ancestry consistent with the positive D(San, Yoruba, Neander, Chimp) statistics for all panels except their own; the negative statistics for their own panel is due to their archaic African ancestry which makes them less like Neandertals.

I conjecture that different archaic populations have contributed polymorphism to different African populations.

This question can be addressed empirically on the basis of whole genome sequence data. The Out-of-Africa bottleneck hypothesis suggests that reduced polymorphism in non-Africans is due to loss of variation as a limited number of founders exited Africa, carrying a subset of African variation. If Africans are descended primarily from the modern human groups left behind, then they will all carry the same "missing variation" set not found in Eurasians.

On the other hand, if, as I suggest, modern human groups encountered and admixed with different divergent African hominins, then different African populations will carry substantially disjoint sets of variants, reflecting deep population structure within Africa itself. Time will tell whether this prediction will prove to be true.

ADMIXTURE analysis of Schlebusch et al. (2012) data

The ADMIXTURE analysis of Schlebusch et al. (2012) did not include Eurasian references, but thanks to the fact that the authors have made their data publicly available, anyone can carry out additional analyses on it. I am sure that this data will be very useful in the future. The list of included populations, with sample sizes are:

• ColouredColesberg_Sch 20
• ColouredWellington_Sch 20
• Khomani_Sch 39
• Karretjie_Sch 20
• Khwe_Sch 17
• GuiGhanaKgal_Sch 15
• Juhoansi_Sch 18
• Nama_Sch 20
• Xun_Sch 19
• SEBantu_Sch 20
• SWBantu_Sch 12

As is my convention, the _Sch ending denotes that these populations are from the Schlebusch et al. paper

As always with a new dataset, after processing it, I ran a quick test to make sure everything seemed to be alright. This time, I included the 220 individuals in the released datasets together with 28 HGDP Sardinians and 10 HGDP Dai, and ran a quick K=4 ADMIXTURE analysis:

These appear to make sense. The "green" Dai-like element in the Coloured samples is probably a stand-in for Indian ancestry in that population. The plot of individuals shows considerable variation within several populations:

Complex origins and natural selection of the Khoe-San

The Khoe-San were recently made the object of a study by Pickrell et al. in a paper that was posted on arXiv and ought to appear in journal form in the near future. Good things come in pairs, so on the heels of that study, a new paper in Science by Schlebusch et al. deals with a similar set of populations. The former paper used the Affymetrix Human Origins Array which contains sets of SNPs ascertained in different individuals from around the world, and the dataset will be comparable to the HGDP set genotyped on the same chip. The current study uses the Illumina Omni 2.5, which would make its data to comparable to the 1000 Genomes data, as well as to a variety of other data genotyped on Illumina platforms. So, from the data perspective, I would say that the two nicely complement each other.

There is an abundance of good stuff in the 176 pages of supplementary material which are freely available in the Science website.

One important technical proposition in the paper is the use of a concordance ratio. As I understand it, this is based on the idea that when populations split, initially the signal that they did so is very weak, and becomes stronger with more time (and drift). So, by taking the ratio of concordant minus discordant alleles over concordant plus discordant ones, they can show support for a topology and estimate population split times.

Of course, Khoe-San populations cannot really be seen as having split from the rest of mankind at some particular time. Pickrell et al. argue for this on the basis of admixture LD in even the most "unadmixed" populations (such as HGDP San), but the most obvious reason why the simple split scenario cannot be true comes from the fact that the Khoe-San possess a substantial percentage of Y-haplogroup E, which links them to other Sub-Saharan Africans, and even Eurasians within a ~50ka framework at most, and probably much lower, since they carry derived sublineages within E that were founded much more recently.

Nonetheless, this admixture was probably not so great to destroy the evidence of isolation, and the authors give an estimate of ~100ka for the split:

This division forms the deepest divergence among extant humans (Fig. 2A, S32) and, assuming an effective population size (Ne) of 21,000 individuals (11, 12), the maximum likelihood divergence time is Ts = 0:083 × 2Ne generations (95% ML CI: 0.075-0.091) corresponding to ∼100,000 years ago (14), in agreement with previous estimates of 110,000-160,000 years ago (11, 12).

But, this estimate disagrees with the idea that Khoe-San split off 250-300 thousand years ago, which has been advanced on the basis of the slower autosomal mutation rate. Many of the news headlines on the paper talk about the paper showing that Khoe-San diverged before Out-of-Africa, but, actually, using the new slow mutation rate, a date of 100ka is actually around the time, or even after Out-of-Africa, which now appears to have taken place twice as early as previously thought.

Thankfully, Schlebusch et al. do not only give absolute age estimates, but also express their age estimates in terms of the effective population size. But, the effective population size is indirectly linked to the autosomal mutation rate, as I noted in my review of Gronau et al. and Veeramah et al., i.e. the two papers cited for the effective population size of 21,000 individuals. In order to generate the same amount of genetic divergence, a slower mutation rate requires a higher population size. Ergo, I don't think the estimates of Schlebusch et al. are discordant with those of Scally and Durbin, and, the two may harmonize once effective population sizes are re-calculated on the basis of the slow human autosomal mutation rate.

The authors do acknowledge the possibility of archaic admixture in Africa. In my opinion, the presence of this admixture can harmonize the evidence of shallow common ancestry with Eurasians and African farmers (e.g., in the form of Y-haplogroup E) with the deep autosomal divergence times.

I am also looking forward to getting the new data when it appears at the Jakobsson lab data page. Together with the HGDP San (on both Affymetrix and Illumina platforms), and the Henn et al. data, there will shortly be no shortage of data on the Khoe-San. And, together with the data from Pagani et al. on Ethiopia it may be a good idea to update my africa9 calculator when I find the time for it.

Science DOI: 10.1126/science.1227721

Genomic Variation in Seven Khoe-San Groups Reveals Adaptation and Complex African History

Carina M. Schlebusch et al.

The history of click-speaking Khoe-San, and African populations in general, remains poorly understood. We genotyped ~2.3 million SNPs in 220 southern Africans and found that the Khoe-San diverged from other populations >=100,000 years ago, but structure within the Khoe-San dated back to about 35,000 years ago. Genetic variation in various sub-Saharan populations did not localize the origin of modern humans to a single geographic region within Africa; instead, it indicated a history of admixture and stratification. We found evidence of adaptation targeting muscle function and immune response, potential adaptive introgression of UV-light protection, and selection predating modern human diversification involving skeletal and neurological development. These new findings illustrate the importance of African genomic diversity in understanding human evolutionary history.

Link

Out-of-Asia and Into-Africa (?)

The publication of version 2 of the Pickrell et al. paper on South Africa is as good an opportunity as any to discuss something anew something that I've been hinting at for some time now.

First things first: Pickrell et al. find West Eurasian admixture in the Hadza and Sandawe:

Both of these are consistent with west Eurasian (either European or, more likely, Arabian), gene  ow into these populations. To further examine this, we turned to ROLLOFF. We used Dinka and French as representatives of the mixing populations (since date estimates are robust to improperly speci ed reference populations). The results are shown in Supplementary Figure S22. Both populations show a detectable curve, though the signal is much stronger in the Sandawe than in the Hadza. The implied dates are 89 generations ( 2500 years) ago for the Hadza and 66 generations ( 2000 years) ago for the Sandawe. These are qualitatively similar signals to those seen by Pagani et al. [65] in Ethiopian populations.

The presence of West Eurasian ancestry in the Hadza and Sandawe was anticipated in my world9 calculator, where both these populations were shown to possess Caucasoid admixture entirely of the "Southern" component. This component peaks in Arabia, and is unaccompanied by any other type of Caucasoid element really only there. So, it is very likely that there was indeed such a migration into East Africa. What Pickrell et al. have added to our knowledge is that this migration is fairly recent.

Razib repeats one of his favorite analogies about events taking place in Africa after the pyramids were rising in Egypt. I will use a Greek epic analogy, by pointing out that at the time that Memnon the Ethiopian led his contingent to the aid of Troy, these events had not yet taken place.

Depictions of Memnon changed during classical antiquity, from a Caucasoid norm, as in the red-figure kylix on the left, to a more stereotypically African form by Roman times. This is sometimes taken as simply a consequence of the fact that the ancient Greeks were unfamiliar with African phenotypes, and changed their portraiture of Ethiopians as they became more familiar with them during Hellenistic and Roman times.

But, the very name of Aithiopes first attested in Homer (8th c. BC) attests to the fact that the Greeks were aware of what Ethiopians looked like, at least in terms of their dark pigmentation. And, there are depictions of Africans in classical art, as well as a famous quote in Herodotus which makes abundantly clear that he was aware of the physical characteristics of what we would call "Sub-Saharan Africans".

We don't only need to look at Ethiopia for evidence of the strange events that were taking place in Africa during classical antiquity. A great punch-in-the-face reminder of these events comes from the much later Greek author Pausanias who records that a statue of Athena he observed in Attica had blue eyes which he ascribed to the Libyan origin of her myth. How strange it seems to us that one would look to Africa for an explanation for the blue-eyed goddess.

Libya was of course, the ancient name for Africa, and especially Africa west of Egypt, what we might call Berber-land. Egypt was often reckoned by the ancient as part of Asia. In any case, Pausanias' strange assertion finds support in the Egyptian monuments that really do depict the ancient Libyans (=Berbers) as Caucasoid, and often lighter than Middle Eastern people. This would also accord with Coon's famous discovery of "Irish-like" Berbers among the Riffians; I often dismissed such assertions, but in a landscape of human prehistory that is getting stranger by the month, it is worth digging for gold nuggets in old texts.

A recent study claimed that there was back-to-Africa gene flow into Eurasia more than 12,000 years ago. On the other hand, both HAPMIX and StepPCO estimate the admixture in Mozabite Berbers as taking place ~120 generations ago, or, about 3.5kya assuming a generation length of 29 years as Patterson et al. (2012) do. I have observed that rolloff produces generally lower dates than these two methods, so I would not be surprised if that is the case here as well.

It seems that as recently as a few thousand years ago, West Eurasian populations were moving into Africa from both north and east. As Pickrell et al. have discovered, their eastern branch also contributed to South Africans, tagging along the dispersal of pastoralists from East-to-South Africa.

The big question is: did West and Central Africa escape this population movement?

I seriously suspect that it did not. I base that assertion on several arguments, of varying strength:

1. Why would they? If they inundated East and North Africa, why would they not venture further?
2. Living Sub-Saharan African farmers are not symmetrically related to West and East Eurasians: they are closer to the former. West Eurasian back-migration would explain this phenomenon.
3. The Great Event in Sub-Saharan Africa was doubtlessly the Bantu explosion, and it is a curious coincidence that this took place precisely close to the time of these events
4. The Iwo Eleru crania from Nigeria are of late Pleistocene age, archaic in character, and unlike modern West Africans. Something did happen in West Africa over the course of, say, the last 10,000 years

And, I always try to remind myself of the Kiffians and Tenerians. I have not seen any follow-up work on them, but if anyone has an ancient DNA lab, I'd think they would be prime candidates for a study.

Speaking of ancient DNA, this unexpected archaeogenetic study from the University of Khartoum, hints at important changes in Africa:

The area known today as Sudan may have been the scene of pivotal human evolutionary events, both as a corridor for ancient and modern migrations, as well as the venue of crucial past cultural evolution. Several questions pertaining to the pattern of succession of the different groups in early Sudan have been raised. To shed light on these aspects, ancient DNA (aDNA) and present DNA collection were made and studied using Y-chromosome markers for aDNA, and Y-chromosome and mtDNA markers for present DNA. Bone samples from different skeletal elements of burial sites from Neolithic, Meroitic, Post-Meroitic and Christian periods in Sudan were collected from Sudan National Museum. aDNA extraction was successful in 35 out of 76 samples, PCR was performed for sex determination using Amelogenin marker. Fourteen samples were females and 19 were males. To generate Y-chromosome specific haplogroups A-M13, B-M60, F-M89 and Y Alu Polymorphism (YAP) markers, which define the deep ancestral haplotypes in the phylogenetic tree of Y-chromosome were used. Haplogroups A-M13 was found at high frequencies among Neolithic samples. Haplogroup F-M89 and YAP appeared to be more frequent among Meroitic, Post-Meroitic and Christian periods. Haplogroup B-M60 was not observed in the sample analyzed.

I was reminded of it recently when this curious abstract came up, which I still believe is missing a zero somewhere, but these days you never know.

Evidence that Sub-Saharan Africans too have experienced gene flow from West Eurasians occasionally comes up, but formal tests of admixture, e.g., f3(Yoruba; San, French) usually do not achieve significance. But, we must be cautious: South Africans do appear admixed between San and East Africans, but this is a consequence of the fact that admixture is recent, leaving a trail of populations of varying East African ancestry, and the San still exist and can serve as one pole in a comparison of admixture.

David Reich has hinted at dual origins for West Africans. I am looking forward to learning what he means by it, but I would not be surprised if it involves admixture between a Eurasian-like population with a Palaeoafrican population of indigenous West African hunter-gatherers.

In any case, ex Africa semper aliquid novi even today. But, interdum, aliquid novum in Africam.

UPDATE: Pickrell and co-authors discuss their paper here.

In favor of recent Out-of-Africa (Eriksson et al. 2012)

A new paper in PNAS argues for a recent (~60kya) expansion of modern humans Out-of-Africa. After reading the title, I was not sure what date the authors were arguing for, and I went straight for the movie in the supplemental material, which is a pretty cool depiction of the authors' scenario.

However, I disagree with the conclusions of this paper, for a variety of reasons. First, the climate history of Africa is consistent with older dispersal scenarios. The authors of the current paper follow other researchers into attributing the Skhul/Qafzeh hominins to an Out-of-Africa-that-failed, but that proposition is increasingly untenable.

The halving of the human autosomal mutation rate implies that Eurasians and Africans split before 100 thousand years ago, and African hunter-gatherers may have split as much as 300 thousand years ago. These dates are not set in stone, but can be downsized if one allows for substantial archaic African admixture. But, doing so weakens the case for a sub-Saharan origin of Homo sapiens.

Second, the Nubian Complex is a direct archaeological link between NE Africa and S Arabia pre-100ka. It becomes increasingly difficult to argue that the pre-100ka expansion fizzled when you have the triple evidence of Mt. Carmel, the Nubian Complex, and Jebel Faya, providing a combination of anthropological and archaeological evidence for African-Asian interaction prior to 100ka.

Some of the conclusions of this paper may be influenced by their choice of the dinucleotide mutation rate:

The dinucleotide stepwise mutation model mutation rate for these markers was estimated in the work by Dib et al. (46) to μdi = 1.52 × 10−3 mutations per generation.

But, Sun  et al. seem to report a much slower dinucleotide mutation rate, as well as a deviation from the stepwise symmetrical model that would bias age estimates downwards if that model is used. So, I am not very confident in the age estimates provided in this paper.

There is a good reason to favor a recent human expansion: if Out-of-Africa happened pre-100ka, as I have argued, then what did modern humans wait for to conquer the rest of the planet (a greater than 50ka hiatus until they begin appearing all over Eurasia). However, that problem can be solved if we acknowledge the fact that modern humans prior to 100ka may have been anatomically "like us", but behaviorally they were not much different from other hominins living on the planet at the time. These pre-100ka H. sapiens were just another set of hunter-gatherers: they may have had a chin, a smaller face, and a more globular braincase, but they did not appear to behave in any drastically different way than other humans who lacked these features.

There are three factors that drive migration: curiosity, need, and ability. One may wonder "what's on the land beyond the sea", but one needs the ability to build a lasting boat to find out. One may have the ability to build a boat, but has no need to do so, if there is game-a-plenty around camp and a beautiful woman with a few beautiful babies in the shelter.

I think that 2-3 reasons contributed to the hiatus:

1. The going was good in Arabia prior to the climate crisis of ~70kya
2. The way north was blocked by Neandertals
3. Whether or not modern humans had the genetic capacity to outcompete the Neandertals, they did not yet have the behavioral expression needed to achieve this

I don't know to what extent changes in the modern human lineage made the mental hardware of early Homo sapiens something like a transistor-based computer that had to compete against the older triode-based models that filled the planet. As we sample more ancient hominins, we may eventually find out whether our wiring was really much improved.

But, one does not really need the best of wiring to conquer a planet. Few would argue today, I suspect, that English mental hardware was superior to e.g., Bavarian mental hardware, but the English brought half the planet under their domination, partly because of their fortunate geographical position which gave them (and other West Europeans) access to the lands beyond the sea. Similarly, few would argue that the Mongols had an innate ability to conquer half of Eurasia, but they happened to have a combination of drive, leadership, organization, and military hardware that allowed them to do so.

This is what I suspect was the real cause for the success of modern humans: they may have had some genetic advantage over others, but their success was partly unintended (the consequence of the drying up of the Sahara-Arabia region that forced them out c. 70kya), and partly the result of them having some vital technological "edge" over other Homo populations.

There may have been interplay between the "need" and "ability" causes of the great human diaspora: as modern humans were pushed out by the advancing desert, they had to adapt to dwindling resources, the challenge of new environments, and the challenge of contact and competition with archaic hominins in both Eurasia and Africa. Adversity does not always breed success: it most often results in failure. But, while many long-forgotten peoples may have faced formidable challenges during the long aeons of geological time, at least one of them had the combination of luck and the "right stuff" to rise to the occasion, and we are their descendants.


PNAS doi: 10.1073/pnas.1209494109

Late Pleistocene climate change and the global expansion of anatomically modern humans

Anders Eriksson et al.

The extent to which past climate change has dictated the pattern and timing of the out-of-Africa expansion by anatomically modern humans is currently unclear [Stewart JR, Stringer CB (2012) Science 335:1317–1321]. In particular, the incompleteness of the fossil record makes it difficult to quantify the effect of climate. Here, we take a different approach to this problem; rather than relying on the appearance of fossils or archaeological evidence to determine arrival times in different parts of the world, we use patterns of genetic variation in modern human populations to determine the plausibility of past demographic parameters. We develop a spatially explicit model of the expansion of anatomically modern humans and use climate reconstructions over the past 120 ky based on the Hadley Centre global climate model HadCM3 to quantify the possible effects of climate on human demography. The combinations of demographic parameters compatible with the current genetic makeup of worldwide populations indicate a clear effect of climate on past population densities. Our estimates of this effect, based on population genetics, capture the observed relationship between current climate and population density in modern hunter–gatherers worldwide, providing supporting evidence for the realism of our approach. Furthermore, although we did not use any archaeological and anthropological data to inform the model, the arrival times in different continents predicted by our model are also broadly consistent with the fossil and archaeological records. Our framework provides the most accurate spatiotemporal reconstruction of human demographic history available at present and will allow for a greater integration of genetic and archaeological evidence.

Link

Longer time scale for human evolution (Hawks 2012)

Scally and Durbin published a recent review on the implications of a slower human autosomal mutation rate, and now John Hawks has a commentary on the same topic in PNAS (pdf; paywall). He goes through a lot of the evidence of early fossil hominins and ape and mentions several examples that harmonize with the slower mutation rate. As expected, he also finds a better agreement of the slow mutation rate with the evidence for Neandertals where 530,000 year old finds from Atapuerca show signs of belonging to the Neandertal lineage, a date that is inconsistent with a late divergence of modern humans and Neandertals. Finally, he has this to say about modern humans:

Across this same time scale, the archaic ancestors of today’s Africans had already developed an intricate population structure. Genomic investigation of African hunter–gatherers has opened new windows onto this deep genetic history of differentiation and introgression (14, 15), bringing the origin of modern African diversity into the population structure of the early Middle Pleistocene. A simple hypothesis of modern human origins in a bottlenecked population cannot account for this diverse genetic history.    

The mtDNA time scale now poses a hanging question. Mitochondrial mutations occur much more often than nuclear DNA mutations, with greater heterogeneity among sites (16). Still, our estimate of mtDNA substitution rates depends on our estimates of branch lengths of the primate phylogeny. Until now, mitochondrial comparisons have been the strongest evidence in favor of a short time scale for the dispersal and differentiation of non-African peoples, within the past 70,000 y (17). Some recent attempts to examine the relationships of non-African populations using nuclear genome data have led to time scales in excess of 100,000 y (18), and others favor more recent estimates (19). Despite the recency of this work, most authors have continued to use an outdated fast molecular clock and short generation time estimates. As we move forward, such results will need to be corrected or adjusted to enable comparisons with current work. 

There is a very interesting question here, which I've mentioned before, but is worth repeating: admixture between divergent lineages can inflate split times. Acceptance of the slow autosomal mutation rate will result in split times in excess of 100 thousand years for Africans vs. non-Africans, and perhaps 300 thousand years for African hunter-gatherers. On the other hand, the mtDNA clock (haplogroup L3 = 70ky), no matter how it is recalibrated is unlikely to match these old dates, and the Y-chromosome clock (current estimate of its root a little more than 100 ky, and of the dominant African lineage E on the cusp of the LSA) will certainly not match them.

In my opinion, it will slowly become apparent that the way to harmonize our picture of human origins is to accept a substantial degree of archaic admixture in Africa. Such admixture cannot be detected directly, because there are no archaic genomes from Africa, and the hot climate throughout much of the continent may make preservation of DNA more difficult than in northern parts of Eurasia (where Neandertal and Denisovan individuals were from). Nor can it always be detected with LD-based methods, since LD decays exponentially and really old admixture is indistinguishable from an excess of mutation in a large population size. But, its acceptance will simultaneously solve the riddle of excess polymorphism in Africans, remove the need for an Out-of-Africa bottleneck of biblical proportions, and resolve the discrepancy between autosomal and uniparental evidence.