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Review
, 136 (5), 529-546

The Study of Human Y Chromosome Variation Through Ancient DNA

Affiliations
Review

The Study of Human Y Chromosome Variation Through Ancient DNA

Toomas Kivisild. Hum Genet.

Erratum in

Abstract

High throughput sequencing methods have completely transformed the study of human Y chromosome variation by offering a genome-scale view on genetic variation retrieved from ancient human remains in context of a growing number of high coverage whole Y chromosome sequence data from living populations from across the world. The ancient Y chromosome sequences are providing us the first exciting glimpses into the past variation of male-specific compartment of the genome and the opportunity to evaluate models based on previously made inferences from patterns of genetic variation in living populations. Analyses of the ancient Y chromosome sequences are challenging not only because of issues generally related to ancient DNA work, such as DNA damage-induced mutations and low content of endogenous DNA in most human remains, but also because of specific properties of the Y chromosome, such as its highly repetitive nature and high homology with the X chromosome. Shotgun sequencing of uniquely mapping regions of the Y chromosomes to sufficiently high coverage is still challenging and costly in poorly preserved samples. To increase the coverage of specific target SNPs capture-based methods have been developed and used in recent years to generate Y chromosome sequence data from hundreds of prehistoric skeletal remains. Besides the prospects of testing directly as how much genetic change in a given time period has accompanied changes in material culture the sequencing of ancient Y chromosomes allows us also to better understand the rate at which mutations accumulate and get fixed over time. This review considers genome-scale evidence on ancient Y chromosome diversity that has recently started to accumulate in geographic areas favourable to DNA preservation. More specifically the review focuses on examples of regional continuity and change of the Y chromosome haplogroups in North Eurasia and in the New World.

Conflict of interest statement

I declare no conflict of interests.

Figures

Fig. 1
Fig. 1
Effect of low coverage of the data and post-mortem damage on the inferences of branch lengths and on the phylogenetic mapping of mutations to the tree. A general example of phylogenetic relationships between one high coverage modern (M1) and two low coverage ancient (A1 and A2) samples is shown. The number of mutations mapping to each branch is shown on both trees. The change in numbers of mutations mismapped due to low coverage on each branch of the tree is explained with the red arrows that indicate the directionality of the mismapping. A1 is shown to carry more damage-induced mutations than A2. Modified from Poznik et al. (2016), Supplementary Figure 18
Fig. 2
Fig. 2
Phylogenetic mapping of a low-coverage ancient DNA sequence to a tree drawn from a general example of a data set of high coverage sequences of modern samples. Left panel shows the tree inferred from modern samples. Middle section shows the mapping of a sample sequenced by shotgun approach. The right panel shows the mapping of the same sample to the tree following SNP-targeted capture approach where modern samples 1 and 3 had been used in the capture design
Fig. 3
Fig. 3
Human Y chromosome diversity outside Africa 20–50 thousand years ago. The branching structure of 41 extant Y chromosome clades inferred to be older than 30,000 years is shown according to the tree based on high coverage Y chromosome sequences presented in Karmin et al. (2015), Figure S9. The phylogenetic mapping to this tree of nine late Pleistocene ancient Y chromosomes that predate the Last Glacial Maximum—from Ust’Ishim (Fu et al. 2014), Oase (Fu et al. 2015), Kostenki (Seguin-Orlando et al. 2014), Malt’a (Raghavan et al. 2014b), Dolní Věstonice, Goyet, and Paglicci (Fu et al. 2016) sites—is shown in red. The zoomed in version of the sub-tree relating Oase, Ust’Ishim with extant variation of the N, O and NO2 clades is shown with branch-defining marker names [modified from (Poznik et al. 2016)] next to the geogrpaphic map displaying the locations of the four ancient sites. The colour-coded distribution of Y chromosome haplogroups in present day populations ignores cases of recent admixture. Haplogroup names here and in other figures follow the nomenclature suggested in Karmin et al. (2015)
Fig. 4
Fig. 4
Major sub-clades of Y chromosome haplogroup C in ancient and present-day populations. The structure of the major sub-clades is drawn in proportion to their coalescent time (the tip of each triangle) estimated from high coverage genomes of present-day populations (Bergstrom et al. ; Karmin et al. ; Poznik et al. ; Scozzari et al. 2012). The phylogenetic mapping of ancient Y chromosomes (Gamba et al. ; Mathieson et al. ; Olalde et al. ; Seguin-Orlando et al. 2014) is shown with red symbols. Haplogroup names are shown in brown font and haplogroup-defining SNP-marker names in grey font next to relevant branches. The key areas of the present-day spread of the haplogroups are indicated with colour and white text inside the triangles. PNG Papua New Guinea
Fig. 5
Fig. 5
Major sub-clades of Y chromosome haplogroups G and H in ancient and present-day populations. The structure of the major sub-clades is drawn in proportion to time according to estimates from high coverage genomes of present-day populations (Hallast et al. ; Karmin et al. ; Poznik et al. 2016) http://isogg.org/tree/, https://www.yfull.com/). The phylogenetic mapping of ancient Y chromosomes (Allentoft et al. ; Broushaki et al. ; Fu et al. ; Gunther et al. ; Haak et al. ; Hofmanova et al. ; Lazaridis et al. , ; Mathieson et al. 2015) is shown with red symbols. Haplogroup-defining marker names are shown in grey font next to relevant branches
Fig. 6
Fig. 6
Major sub-clades of Y chromosome haplogroups I and J in ancient and present-day populations. The structure of the major extant sub-clades of haplogroups I and J is shown by triangles the tips of which are drawn in proportion to time according to coalescent time estimates from high coverage genomes of present-day populations (Hallast et al. ; Karmin et al. ; Poznik et al. 2016) http://isogg.org/tree/, https://www.yfull.com/). The colour of each triangle reflects the main geographic areas of its spread according to the map shown in the middle of the plot. The phylogenetic affiliations of ancient Y chromosomes (Allentoft et al. ; Gamba et al. ; Gunther et al. ; Haak et al. ; Hofmanova et al. ; Jones et al. ; Lazaridis et al. ; Mathieson et al. ; Skoglund et al. 2012) are shown with red symbols. Haplogroup-defining marker names are shown in grey font next to relevant branches
Fig. 7
Fig. 7
Major sub-clades of Y chromosome haplogroups R1a and R1b in ancient and present-day populations. The structure of the major extant sub-clades of haplogroups R1a and R1b is shown by triangles the tips of which are drawn in proportion to time according to coalescent time estimates from high coverage genomes of present-day populations (Batini et al. ; Cruciani et al. ; Hallast et al. ; Karmin et al. ; Poznik et al. 2016), http://isogg.org/tree/, https://www.yfull.com/). The colour of each triangle reflects the main geographic areas of its spread according to the map shown in the middle of the plot. The phylogenetic affiliations of ancient Y chromosomes chromosomes (Allentoft et al. ; Broushaki et al. ; Cassidy et al. ; Haak et al. ; Jones et al. ; Lazaridis et al. ; Mathieson et al. ; Schiffels et al. 2016) are shown with red symbols. Haplogroup-defining marker names are shown in grey font next to relevant branches. Four Yamnaya, one Samara Bronze Age and two Nordic Bronze Age R1b-M269 samples could not be placed on the tree as they lacked coverage at M412, L11, and Z2105 SNPs
Fig. 8
Fig. 8
The main branches of Y chromosome haplogroup Q in ancient and present-day populations. The structure of the major sub-clades is drawn in proportion to time according to estimates from high coverage genomes of present-day populations (Karmin et al. ; Poznik et al. 2016), http://isogg.org/tree/ISOGG_HapgrpQ.html, https://www.yfull.com/tree/Q/). The phylogenetic mapping of ancient Y chromosomes (Kemp et al. ; Rasmussen et al. 2010, 2014, 2015) is shown with red symbols. Haplogroup-defining marker names are shown in grey font next to relevant branches

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