With this study, analyses of two independently inherited DNA markers, the only two studies based on global samples of dogs performed so far, give strikingly similar pictures of dog phylogeography. Thus, both the present study of Y-chromosomal DNA and earlier studies of mtDNA (Pang et al., 2009
) show that ~50% of dog genetic diversity is shared in a universal gene pool, but whereas most regions harbour only these 50%, ASY has virtually the full range of genetic diversity from which the complete gene pools in other regions may derive. It is unlikely that the two datasets would by chance have obtained the same phylogeographical pattern or that selection would have affected both markers similarly. Therefore, these results offer strong evidence that domestication of wolf occurred primarily and possibly exclusively in ASY, with only small genetic contributions from wolf in other regions, through dog–wolf hybridisation.
This is in conflict with conclusions normally drawn from analyses of the archaeological record (Clutton-Brock, 1995
) and in a recent study of autosomal SNPs (Vonholdt et al., 2010
), suggesting SW Asia and/or Europe as the principal regions of origin. However, both the archaeological record and the SNP study suffer from geographical bias in a lack of data from ASY (Klütsch and Savolainen, 2011
). Therefore, there is a clear possibility that these datasets failing to identify ASY's central role in dog origins may reflect the lack of sampling specifically from this region. Arguably, the Y-chromosome DNA and mtDNA datasets represent only two genetic markers, and the Y-chromosome data includes relatively small samples. Therefore, analyses of further markers are desirable; when based on comprehensive sampling, large-scale studies of genome wide polymorphisms, for example, autosomal SNPs will help to reveal dog history in unprecedented detail. However, in the light of the mtDNA and Y-chromosomal data, comprehensive sampling from ASY is necessary for any study aimed at unravelling the origins and earliest history of dogs. It is especially notable that, for both Y-chromosome and mtDNA data, diversity is much lower in N China and Central China than in ASY, and instead more similar to that of other regions, for example, SW Asia. Therefore, samples from China or East Asia in general cannot compensate for lack of samples from ASY.
The exact geographical origin of each Y-chromosome haplogroup cannot be determined based on the present dataset. However, it seems clear that at most 50% of the genetic diversity can have originated from SW Asia or from Europe, and it is possible, especially considering that all haplotypes of the four principal haplogroups differ by at most a single substitution from a haplotype found in ASY, that 100% of the Y-chromosome gene pool originated in ASY in a single domestication event. The strongest indication against this is the high frequency and relatively high diversity of HG23 in SW Asia. In Fertile Cr >50% of the samples had HG23 and four of the six haplotypes were represented, suggesting the possibility of a separate origin of HG23, through independent domestication or crossbreeding of dog and wolf. However, in the case of independent domestication a high frequency would be anticipated also in the neighbouring regions, but instead the frequency of HG23 was exceptionally low in, for example, Europe (6%). Considering the large impact of the spread of farming and the related farm animals from the SW Asia to Europe (Bellwood, 2005
), it would be anticipated that European dogs, if originating from SW Asia, would have a high frequency of the SW Asian haplotypes. An alternative possibility is that HG23 originated from crossbreeding of dog with wolf in SW Asia. The mtDNA data gives a clear indication of crossbreeding in SW Asia, haplogroup d2 being found only in SW Asia and the Mediterranean at a frequency of ~2% (Pang et al., 2009
; Klütsch et al., 2010
). However, in crossbreeding of wolf into an already established dog population the novel haplotypes would be expected to remain at low frequency, like the mtDNA haplogroup d2, and not above 50% as HG23. The geographical origin of HG23 is therefore unclear, but an origin in ASY, where three different HG23 haplotypes were found among only three dogs, cannot be excluded.
There was not a single example of regionally restricted Y-chromosome haplogroups and therefore no clear sign that crossbreeding between male wolf and female domestic dog have contributed extensively to the evolution of the domestic dog. However, haplotypes deriving from crossbreeding would normally have limited geographical spread unless a superior phenotype would have evolved (Pang et al., 2009
; Klütsch et al., 2010
), and may have gone undetected in this study. So far, the only clear genetic evidence of wolf–dog crossbreeding is the regionally restricted mtDNA haplogroups d1 (restricted to Scandinavia), d2 (restricted to the Middle East and the Mediterranean), and F (found only in a few extant Japanese dogs and samples from extinct Japanese wolf) (Ishiguro et al., 2009
; Pang et al., 2009
; Klütsch et al., 2010
Care was taken to obtain extensive and representative samples from each geographical region, by collecting across the regions and normally a single sample from each location. It is therefore noticeable that several extensive regions had one haplotype at very high frequency (See Supplementary Dataset 3
), a pattern not seen for mtDNA (Pang et al., 2009
). For example, 6 of 10 samples from across Iran carried haplotype H23*
, all 4 samples from (different parts of) the Japanese main island Honshu, carried H5 and 2 out of 2 samples from each of the South Chinese provinces Guizhou and Hunan carried H6. At analysis of Y-chromosome microsatellites according to (Bannasch et al., 2005
) all samples had different haplotypes (See Supplementary Text
), showing that the sharing of SNP-based haplotypes is not the result of events in modern time. Therefore, the dominance of a single Y-chromosome haplotype across large regions possibly reflects involvement of relatively few males in some migrations and population founder events.
Considering the intense breeding of European dogs during the last few 100 years, giving severe breed-specific bottlenecks (Clutton-Brock, 1995
), special care was taken to avoid sampling bias by sampling a single individual per breed, from different morphological types and from across Europe. The extremely low diversity, 81% of European dogs carrying HG1, must therefore stem from before breeding started, as it is unlikely that all haplogroups but HG1 would have been lost independently in several different lineages leading to today's breeds. For mtDNA the picture is even clearer, with the European population lacking 6 of the 10 principal haplogroups, 5 of which are missing also in SW Asia (Pang et al., 2009
), showing that the loss of diversity occurred before the European and SW Asian populations were originally formed. Therefore, the low genetic diversity of the European population, and its separate grouping in analysis of autosomal SNPs (Vonholdt et al., 2010
), seem to reflect the geographical position at the far end of the Eurasian continent compared with ASY, rather than recent intense breeding.
The Y-chromosome data, as well as mtDNA (Pang et al., 2009
) and autosomal MHC data (Vilà et al., 2005
), indicates that a large number of wolves were founders for the domestic dog population. Considering the relatively small sample of dogs in this study and that some domesticated wolves probably carried identical HTs, a minimum of 13 Y-chromosome haplotypes and 51 mtDNA haplotypes (Pang et al., 2009
) deriving from the wolf founders indicates that the origin of dogs involved taming of several hundred wolves and was a major event in the related human culture.
The phylogeographical data is not detailed enough to indicate exactly where this domestication may have taken place, since several South Chinese provinces and also, for example, Burma have not been analysed for either Y-chromosome DNA or mtDNA. The possibility that dogs originated in connection with the transition from hunter gathering to farming of rice (Bellwood, 2005
) has been suggested, based on mtDNA indicating dogs to have originated approximately at this time (Pang et al., 2009
). This would place the origin of dogs in Northern/Central ASY where the earliest evidence of rice cultivation has been found (Underhill, 1997
; Bellwood, 2005
). However, the highest Y-chromosomal diversity was found in Southw ASY, which was also the only region harbouring the full set of the principal mtDNA haplogroups (Pang et al., 2009
). The southern range of wolves would define the southern limit for possible domestication of wolf, but the historical range of wolf in the region is not known. Thus, although the principal region of dog origins has probably been identified, many details remain to be studied. However, analyses based on denser sampling and application of the new generation of powerful DNA sequence analysis has the potential of producing a very detailed phylogeographic map of the region, promising a detailed picture of the first steps in dog origins.