Refining Y-chromosome phylogeny with South African sequences

bioRxiv http://dx.doi.org/10.1101/034983

Refining the Y chromosome phylogeny with southern African sequences

Chiara Barbieri, Alexander Hübner, Enrico Macholdt, Shengyu Ni, Sebastian Lippold, Roland Schröder, Sununguko Wata Mpoloka, Josephine Purps, Lutz Roewer, Mark Stoneking, Brigitte Pakendorf

The recent availability of large-scale sequence data for the human Y chromosome has revolutionized analyses of and insights gained from this non-recombining, paternally inherited chromosome. However, the studies to date focus on Eurasian variation, and hence the diversity of early-diverging branches found in Africa has not been adequately documented. Here we analyze over 900 kb of Y chromosome sequence obtained from 547 individuals from southern African Khoisan and Bantu-speaking populations, identifying 232 new sequences from basal haplogroups A and B. We find new branches within haplogroups A2 and A3b1 and suggest that the prehistory of haplogroup B2a is more complex than previously suspected; this haplogroup is likely to have existed in Khoisan groups before the arrival of Bantu-speakers, who brought additional B2a lineages to southern Africa. Furthermore, we estimate older dates than obtained previously for both the A2-T node within the human Y chromosome phylogeny and for some individual haplogroups. Finally, there is pronounced variation in branch length between major haplogroups; haplogroups associated with Bantu-speakers have significantly longer branches. This likely reflects a combination of biases in the SNP calling process and demographic factors, such as an older average paternal age (hence a higher mutation rate), a higher effective population size, and/or a stronger effect of population expansion for Bantu-speakers than for Khoisan groups.

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Ancient mtDNA from southern Africa related to San

Genome Biol Evol (2014) doi: 10.1093/gbe/evu202

First Ancient Mitochondrial Human Genome from a Pre-Pastoralist Southern African

Alan G. Morris et al.

The oldest contemporary human mitochondrial lineages arose in Africa. The earliest divergent extant maternal offshoot, namely haplogroup L0d, is represented by click-speaking forager peoples of Southern Africa. Broadly defined as Khoesan, contemporary Khoesan are today largely restricted to the semi-desert regions of Namibia and Botswana, while archeological, historical and genetic evidence promotes a once broader southerly dispersal of click-speaking peoples including southward migrating pastoralists and indigenous marine-foragers. Today extinct, no genetic data has been recovered from the indigenous peoples that once sustained life along the southern coastal waters of Africa pre-pastoral arrival. In this study we generate a complete mitochondrial genome from a 2,330 year old male skeleton, confirmed via osteological and archeological analysis as practicing a marine-based forager existence. The ancient mtDNA represents a new L0d2c lineage (L0d2c1c) that is today, unlike its Khoe-language based sister-clades (L0d2c1a and L0d2c1b) most closely related to contemporary indigenous San-speakers (specifically Ju). Providing the first genomic evidence that pre-pastoral Southern African marine foragers carried the earliest diverged maternal modern human lineages, this study emphasizes the significance of Southern African archeological remains in defining early modern human origins.

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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.

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How some Bantu got clickin' (Barbieri et al. 2012)

Eur J Hum Genet. 2012 Aug 29. doi: 10.1038/ejhg.2012.192. [Epub ahead of print]

Genetic perspectives on the origin of clicks in Bantu languages from southwestern Zambia. 

Barbieri C, Butthof A, Bostoen K, Pakendorf B. Source Max Planck Research Group on Comparative Population Linguistics, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Abstract 

Some Bantu languages spoken in southwestern Zambia and neighboring regions of Botswana, Namibia, and Angola are characterized by the presence of click consonants, whereas their closest linguistic relatives lack such clicks. As clicks are a typical feature not of the Bantu language family, but of Khoisan languages, it is highly probable that the Bantu languages in question borrowed the clicks from Khoisan languages. In this paper, we combine complete mitochondrial genome sequences from a representative sample of populations from the Western Province of Zambia speaking Bantu languages with and without clicks, with fine-scaled analyses of Y-chromosomal single nucleotide polymorphisms and short tandem repeats to investigate the prehistoric contact that led to this borrowing of click consonants. Our results reveal complex population-specific histories, with female-biased admixture from Khoisan-speaking groups associated with the incorporation of click sounds in one Bantu-speaking population, while concomitant levels of potential Khoisan admixture did not result in sound change in another. Furthermore, the lack of sequence sharing between the Bantu-speaking groups from southwestern Zambia investigated here and extant Khoisan populations provides an indication that there must have been genetic substructure in the Khoisan-speaking indigenous groups of southern Africa that did not survive until the present or has been substantially reduced. 

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Khoisan genetic prehistory (Pickrell et al. 2012)

This appears to be the first paper using the specialized Affymetrix chip, which was announced some time ago, and used in some of my previous experiments. The new array has been dubbed "Affymetrix Human Origins array" and has been composed by intersecting panels of SNPs ascertained in individuals from several world populations.

It is of course great to see that this paper has appeared as a preprint in arXiv, and hopefully this is a trend that will continue; biology should be like physics, with papers appearing immediately online for commenting, and not hidden away in authors', editors', and reviewers' drawers for months if not years before they become available to all.

I will highlight some points of particular interest to me:

Some caveats of interpretation here are warranted. First, all the Khoisan populations have some level of admixture with non-Khoisan populations. There is thus no single \split time" in their history, and any method (like the one used here) that estimates a single such time will actually be estimating a composite of several signals. Second, we have made the modeling assumption that history involves populations splitting in two with no gene  ow after the split. More complex demographies are quite plausible, but render the interpretation of a split time nearly meaningless (if populations continue to exchange migrants after \splitting", they arguably have not split at all). We thus consider strong interpretations of split times estimated from genetic data to be impossible, but we nonetheless and the estimates to be useful in constraining the set of historical hypotheses that are consistent with the data. 

This echoes (somewhat) my sentiments about split times being a tug-of-war in the presence of admixture. Another interesting bit from the paper:

Interestingly, a few of the Khoe-speaking populations have slightly positive f4 statistics in this com- parison, and in the Shua the f4 statistic is significantly greater than zero. We speculate that some of the Khoe-speaking populations have a low level of east African ancestry, and that the relevant east African population was itself admixed with a western Eurasian population. The Shua also show a detectable signal of admixture LD, though we estimate the admixture date as much older (44 generations). This signal of east African ancestry specifically in Khoe-speaking populations is of particular interest in the light of the hypoth esis that the Khoe-Kwadi languages were brought to southern Africa by a pre-Bantu pastoralist immigration from eastern Africa [Guldemann, 2008] 

The authors also announce an improvement on TreeMix:

In the original TreeMix algorithm, one first builds the best-tting tree of populations. However, this approach is not ideal if there are many admixed populations (as in our application here, where all of the Khoisan populations are admixed). To get around this, we allow for known admixture events to be incorpo- rated into this tree-building step. Imagine that there are several populations that we think a priori might be unadmixed (in our applications, these are the Chimpanzee, Yoruba, Dinka, Europeans, and East Asians). We  first build the best tree of these unadmixed populations using the standard TreeMix algorithm. Now assume we have an independent estimate of the admixture level of each Khoisan population, and imagine we know the source population for the mixture. 

I don't think that Sub-Saharan African populations can any longer be considered unadmixed. When one used SNPs ascertained in Eurasian individuals, many Sub-Saharan populations appear symmetrically related to Eurasians, because they lack variation at sites where new polymorphism appeared outside Africa. 

This is not, however, the case when one uses SNPs ascertained in African individuals, and a clear pattern of differential affiliation with West Eurasians across the continent is evident. As I have said before, I strongly suspect that this is due to fairly late back-migration of Eurasians into Africa, carrying Y-haplogroup DE chromosomes. Within haplogroup CT, both its major subclades CF and DE are represented in Eurasia, and both D,E, and DE* as well. In Africa, as far as we know, only DE* and E are native. On balance, the weight of the evidence would suggest a Eurasian origin of the DE-YAP haplogroup.

(I would perhaps be as bold as to extend this into the even more basal clades of the phylogeny which turn up with surprising regularity in Eurasian datasets, and are usually discounted as the result of recent admixture. I'm not so sure; if recent admixture was at fault, then the African signal in Eurasia would be absolutely dominated by E-related lineages: but the A's and B's turn up in quite unexpected places. Are they really all recent Africans, or could they share a much deeper common ancestry? If I had deep pockets, I'd surely invest in genome sequencing the collection of such Eurasian erratics)

As a parting thought, I hope that the data used in this paper will become publicly available in time, perhaps when the article appears in journal form. True open science depends not only in the public availability of research results, but also of the data that produced them.

UPDATE: Here is the ADMIXTURE analysis from the paper (Figure 7):

It would have been nice if the Fst values between ancestral populations were reported in the paper; also, if an East Eurasian group was added in the analysis. In any case, there does appear a pattern of differential affiliation with the French population (K=2). At K=3 the main Sub-Saharan (blue) component emerges, and a few populations continue to exhibit an excess of West Eurasian affiliation.

arXiv:1207.5552v1 [q-bio.PE]
The genetic prehistory of southern Africa

Joseph K. Pickrell et al.

The hunter-gatherer populations of southern and eastern Africa are known to harbor some of the most ancient human lineages, but their historical relationships are poorly understood. We report data from 22 populations analyzed at over half a million single nucleotide polymorphisms (SNPs), using a genome-wide array designed for studies of history. The southern Africans-here called Khoisan-fall into two groups, loosely corresponding to the northwestern and southeastern Kalahari, which we show separated within the last 30,000 years. All individuals derive at least a few percent of their genomes from admixture with non-Khoisan populations that began 1,200 years ago. In addition, the Hadza, an east African hunter-gatherer population that speaks a language with click consonants, derive about a quarter of their ancestry from admixture with a population related to the Khoisan, implying an ancient genetic link between southern and eastern Africa.

Link