New papers on human Y-chromosome phylogeny (Poznik et al. and Francalacci et al.)

A couple of important new papers on human Y-chromosome phylogeny appeared in Science today.

Francalacci et al. reconstructs the phylogeny of European Y-chromosomes based on a huge sample of 1,200 Sardinians. Naturally, Sardinians don't have every haplogroup in Europe or the planet, but with such a huge sample it was possible to find almost everything, minus obvious newcomers such as Uralic haplogroup N.

Poznik et al. build a human Y-chromosome phylogeny from 69 male genomes. The main thrust of their paper is to reconcile the "younger" Y-chromosome vs. "older" mtDNA in humans. In my opinion, that ship has sailed with the discovery of Y-haplogroup A00 which now makes the Y-chromosome MRCA of humans ("Adam") much older than the mtDNA one ("Eve").

And, indeed, the fact that the two are of different ages is not particularly troubling or in need of remedy, since for most reasonable models of human origins we do not expect them to be of the same age. Well, unless you believe the latest archaeological models that have early proto-sapiens perfecting their craft by scratching lines and perforating beads in some south African cave before spreading out to colonize the planet in one swift swoop.

The issue of the "discrepancy" aside, Poznik et al. resolve the issue of the binary structure of Y-haplogroup F, by showing that Y-haplogroup G (which is the Iceman's haplogroup, and the lineage most strongly associated with easly European farmers) branches off first from the tree.

Haplogroup G is an unambiguously west Eurasian lineage, so the fact that it is basal within F surely has implications about the origins of this most successful Eurasian group. The pattern is not quite clear, however, because the next most basal branch is H, which is unambiguously South Asian, and the next one after that is IJ vs. K, with IJ again being west Eurasian, with most east Eurasians nested within K. But, if we go up the tree, we see the split of  C (Asian) vs. F (Eurasian), and further up DE (African+Eurasian) vs. CF (Eurasian). It seems to me that apart from the unambiguous African rooting of the entire tree, the rest of the topology paints a picture of a complex peopling of Eurasia, rather than a simple model of successive founder effects.

Another interesting finding of Poznik et al. is the discover of deep substructure within Y-haplogroup A-L419 (bottom of the picture).

The authors arrive at the following mutation rate:

Using entry to the Americas as a calibration point, we estimate a mutation rate of 0.82 × 10−9 per base pair (bp) per year [95% confidence interval (CI): 0.72 × 10−9 to 0.92 × 10−9/bp/year] (table S3).

This is notable for being lower than the directly estimated mutation rate of 1x10-9 of Xue et al. (2009).

The usefulness of "archaeological calibration" eludes me, which brings us back to Francalacci et al. who also archaeologically calibrate their mutation rate and find:

Considering that our analysis focused on approximately 8.97 Mbp of sequence from the Y chromosome X-degenerated region, this rate is equivalent to 0.53 × 10−9 bp−1 year−1.

So, the Francalacci et al. mutation rate is about half that of Xue et al., with that of Poznik et al. being intermediate. The Francalacci et al. rate was calibrated by "the initial expansion of the Sardinian population". Now, whether the current Sardinian population is descended from that initial expansion or from a later successful founder remains to be seen. In any case, using their ultra-slow mutation rate, these authors suggest that:

The main non-African super-haplogroup F-R shows an average variation of 534.8 (±28.7) SNPs, corresponding to a MRCA of ~110,000 years ago, in agreement with fossil remains of archaic Homo sapiens out of Africa (7, 18) though not with mtDNA, whose M and N super-haplogroups coalesce at a younger age (13). The main European subclades show a differentiation predating the peopling of Sardinia, with an average variation ranging from 70 to 120 SNPs (Table 1), corresponding to a coalescent age between 14,000 and 24,000 years ago, which is compatible with the postglacial peopling of Europe.

I am personally skeptical of all such archaeological calibrations and I'd like to see the mutation rate directly estimated using a well-behaved process (say, a 1,000-year old deep pedigree between two modern males separated by 60 meioses). It seems that there is no escape from mutation rate controversies in human genetics.

The most striking piece of data from this paper is the following figure:

Going from left-to-right:

• R2 in Sardinia! This is extremely rare in Europe and underscores the importance of large sample sizes. It'd be wonderful to study it in the future in the context of, say, South Asian R2 which is much more numerous.
• The clear "explosive" expansion of R1b-related lineages
• A very deep common ancestry of haplogroups L and T.
• Quite deep coalescences within Y-haplogroup J
• "Explosive" growth of I2a1a1; this "southwest European" lineage attains its maximum in Sardinia and looks like a clear founder effect. It should definitely be visible in the ancient DNA record of the island.
• Fairly deep splits within G2a. It would be interesting to see how G2 compares with Caucasian G1. We now know that G is very old lineage in West Eurasia (being the first split in haplogroup F), but how much of its present-diversity dates back to splits shortly after the haplogroup's appearance?
• Finally, the deep splits within African haplogroup E correspond to the likely varied origins of these lineages

There's probably much more of interest in these twin papers, so if you notice anything in the supplementary materials, feel free to leave a comment.

Science 2 August 2013: Vol. 341 no. 6145 pp. 562-565

DOI: 10.1126/science.1237619

Sequencing Y Chromosomes Resolves Discrepancy in Time to Common Ancestor of Males Versus Females

G. David Poznik et al.

The Y chromosome and the mitochondrial genome have been used to estimate when the common patrilineal and matrilineal ancestors of humans lived. We sequenced the genomes of 69 males from nine populations, including two in which we find basal branches of the Y-chromosome tree. We identify ancient phylogenetic structure within African haplogroups and resolve a long-standing ambiguity deep within the tree. Applying equivalent methodologies to the Y chromosome and the mitochondrial genome, we estimate the time to the most recent common ancestor (TMRCA) of the Y chromosome to be 120 to 156 thousand years and the mitochondrial genome TMRCA to be 99 to 148 thousand years. Our findings suggest that, contrary to previous claims, male lineages do not coalesce significantly more recently than female lineages.

Link

Science 2 August 2013: Vol. 341 no. 6145 pp. 565-569

DOI: 10.1126/science.1237947

Low-Pass DNA Sequencing of 1200 Sardinians Reconstructs European Y-Chromosome Phylogeny

Paolo Francalacci et al.

Genetic variation within the male-specific portion of the Y chromosome (MSY) can clarify the origins of contemporary populations, but previous studies were hampered by partial genetic information. Population sequencing of 1204 Sardinian males identified 11,763 MSY single-nucleotide polymorphisms, 6751 of which have not previously been observed. We constructed a MSY phylogenetic tree containing all main haplogroups found in Europe, along with many Sardinian-specific lineage clusters within each haplogroup. The tree was calibrated with archaeological data from the initial expansion of the Sardinian population ~7700 years ago. The ages of nodes highlight different genetic strata in Sardinia and reveal the presumptive timing of coalescence with other human populations. We calculate a putative age for coalescence of ~180,000 to 200,000 years ago, which is consistent with previous mitochondrial DNA–based estimates.

Link