A hair-color allele of Neanderthal origin?

 

Taiwanese aboriginal children, Bunun village (source: Jeremy Kemp). 60-70% of Taiwanese aborigines have a loss-of-function allele at the main hair color gene, MC1R, yet their hair is as black as humans with the original “African” allele. This seems to be a general pattern in Asians. They have fewer MC1R alleles than do Europeans, and the ones they have produce the same hair color.

 

When I first wrote about the puzzle of European hair and eye color, a common explanation was Neanderthal admixture. Modern humans intermixed with Neanderthals in Europe, and one legacy of this intermixture is the high prevalence of non-black hair and non-brown eyes we see in present-day Europeans.

I was skeptical. Scientists had already retrieved mtDNA from the remains of Neanderthals and early modern humans, and there was no discernible genetic continuity between the two. Neanderthal admixture seemed minor and could hardly account for the high proportion of Europeans who deviate from the species norm of black hair and brown eyes (Frost, 2006).

With the sequencing of the Neanderthal genome, it became apparent that some admixture had taken place, but only on the order of 1 to 4% in modern Eurasians. Neanderthals did resemble modern humans in having the same main gene for hair color, i.e., MC1R, but the Neanderthal allele at that gene was unlike any allele in modern humans (Lalueza-Fox et al., 2007). Moreover, there was no evidence of the polymorphism that exists for European hair color. The same allele was present in the two Neanderthal individuals that had been sampled.

That seemed to be the end of the story. A new twist, however, has been added by a recent paper. Ding et al. (2014) have found that one of the MC1R alleles in modern humans (Val92Met) appears to be of Neanderthal origin:

In this paper, we present evidences of Neanderthal introgression encompassing the MSH receptor gene MC1R. Furthermore, our evidences support that the derived allele at the functional variant Val92Met of MC1R (i.e., rs2228479*A) is likely of two origins: the vast majority of haplotypes carrying this allele in the human gene pool is resulted from Neanderthal introgression, while one haplotype (NA19084_a) carrying this allele may be from a recurrent mutation in the AMH linage, double recombination, or biased gene conversion.

This finding is consistent with the theory, first advanced by Gregory Cochran, that archaic admixture made it easier for modern humans to adapt to new environments. To be sure, Val92Met is only one of eleven derived MCIR alleles that exist in modern humans. But Ding et al. (2014) also believe that some of these other MC1R alleles are mosaics of Neanderthal and non-Neanderthal segments. So Neanderthal admixture may have helped European hair color to diversify by providing raw material for selection to act on.
 

A silent allele or a silenced allele?

By itself, Neanderthal admixture cannot explain the unusual diversity of hair color in present-day Europeans. It simply provided some of the raw material for this evolutionary development, and in most cases this raw material had to undergo further changes, through mutation and recombination, before it could become useful.

Indeed, despite being a loss-of-function allele, Val92Met seems to produce the same black hair as the original "African" allele. This may be seen in its geographic distribution: ~5% in Europeans, ~30% in continental East Asians, and 60-70% in Taiwanese aborigines (Ding et al., 2014). It has also been reported in South Asians, Papua-New Guineans, Japanese, and Inuit (Harding et al., 2000). Ding et al. (2014) state that this allele is associated with red hair, but the study they cite found only one individual with Val92Met among the 21 redheads examined (Valverde et al., 1995). This proportion is almost identical to the allele's incidence among Europeans in general. More likely than not, that single individual owed her red hair to an allele somewhere else on her genome.

Hair color is much less diverse in Asians, and this is reflected in lower MC1R diversity. Whereas Europeans have eleven MC1R alleles, Asians have only five, and all five produce the same black hair color (Harding et al., 2000). In short, Asians have fewer alleles and proportionately fewer of these differ phenotypically from the ancestral African allele. It looks as if something downstream prevents these alleles from affecting hair color.

As I've argued elsewhere, Europe's diverse palette of hair and eye colors is due to unusual evolutionary circumstances, i.e., intense sexual selection of women within an ecozone (continental steppe-tundra of the last ice age) where almost all food was obtained through long-distance hunting. The consequently higher death rate and lower polygyny rate among hunters dried up the pool of men available for mating and increased competition by women for mates. Women were more strongly selected for eye-catching traits, particularly bright or novel hues, thus creating an increasingly diverse palette of hair and eye colors (Frost, 2006; Frost, 2014).

This ecozone was more suitable for continuous human settlement in Europe than in northern Asia, where it was farther north and farther removed from the moderating influence of the Atlantic. A site in central Siberia from the last ice age has yielded human DNA that shows strong affinities with present-day Europeans and Amerindians, but much less affinity with present-day northern Asians, who seem to be largely the product of repeopling from the south near the end of the last ice age (Maanasa et al., 2014). Europeans have thus better preserved the legacy of this episode of intense sexual selection.

Perhaps the story ends there. Present-day Asians have preserved less of that MC1R diversity and what they have preserved has less functional significance. Or perhaps that diversity was initially functional and then gradually ceased to be functional … because of some other selection pressure? Perhaps, at the end of the last ice age, there was some non-black hair among northern Asians, though much less than among Europeans. Being less common and thus less normal, and no longer favored by intense sexual selection, there may have been stronger social selection to eliminate deviant hair colors.

A similar kind of social selection might explain why red hair is less common than blond hair among Europeans, i.e., stigmatization of redheads that was ultimately due to a mental association between red hair and menstrual blood (Frost, 2012).

There may be a story behind these "silent alleles." 

 

References 

Ding, Q., Y. Hu, S. Xu, C. Wang, H. Li, R. Zhang, S. Yan, J. Wang, and L. Jin (2014). Neanderthal origin of the haplotypes carrying the functional variant Val92Met in the MC1R in modern humans, Molecular Biology and Evolution, published online June 10, 2014

http://mbe.oxfordjournals.org/content/early/2014/06/02/molbev.msu180.abstract

Frost, P. (2006). European hair and eye color - A case of frequency-dependent sexual selection? Evolution and Human Behavior, 27, 85-103. 

Frost, P. (2012). Why are redheads less common than blondes? Evo and Proud, March 10

http://evoandproud.blogspot.ca/2012/03/why-are-redheads-less-common-than.html  

Frost, P. (2014). The puzzle of European hair, eye, and skin color, Advances in Anthropology, 4, 78-88.

http://www.scirp.org/journal/PaperInformation.aspx?PaperID=46104

Harding, R.M., Healy, E., Ray, A.J., Ellis, N.S., Flanagan, N., Todd, C., Dixon, C., Sajantila, A., Jackson, I.J., Birch-Machin, M.A., and Rees, J.L. (2000). Evidence for variable selective pressures at MC1R. American Journal of Human Genetics, 66, 1351-1361. 

Lalueza-Fox, C., H. Römpler, D. Caramelli, C. Stäubert, G. Catalano, D. Hughes, N. Rohland, E. Pilli, L. Longo, S. Condemi, M. de la Rasilla, J. Fortea, A. Rosas, M. Stoneking, T. Schöneberg, J. Bertranpetit,  and M. Hofreiter. (2007). A melanocortin 1 receptor allele suggests varying pigmentation among Neanderthals, Science, 318 (5855), 1453-1455.

http://www.bio.davidson.edu/courses/genomics/Exams/2009/Neaderthal_pigment.pdf  

Maanasa, R., Skoglund, P., Graf, K.E., Metspalu, M., Albrechtsen, A., Moltke, I., Rasmussen, S., Stafford Jr, T.W., Orlando, L., Metspalu, E., Karmin, M., Tambets, K., Roots, S., Mägi, R., Campos, P.F., Balanovska, E., Balanovsky, O., Khusnutdinova, E., Litvinov, S., Osipova, L.P., Fedorova, S.A., Voevoda, M.I., DeGiorgio, M., Sicheritz-Ponten, T., Brunak, S., Demeshchenko, S., Kivisild, T., Villems, R., Nielsen, R., Jakobsson, M., and Willerslev, E. (2014). Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature, 505, 87-91.

http://cteg.berkeley.edu/~nielsen/wordpress/wp-content/uploads/2013/12/Raghavan-M.-et-al.-2013..pdf  

Valverde, P., E. Healy, I. Jackson, J.L. Rees, and J. Thody. (2005). Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans, Nature Genetics, 11, 328-330.

http://www.nature.com/ng/journal/v11/n3/abs/ng1195-328.html

The ancestors with no descendants

Venus of Mal’ta, a figurine from a site in eastern Siberia (source). She comes from a population that was related to modern Europeans and Amerindians but not to modern native Siberians. The Mal’ta Siberians died out at the height of the last ice age and were replaced by people spreading north from East Asia and west from Beringia.

On the eve of the last ice age, Siberia was home to a people who were related to modern Europeans and Amerindians but not to modern native Siberians. So concludes an analysis of DNA from the remains of a boy who lived 24,000 years ago at Mal’ta near Lake Baikal, Siberia.

They found that a portion of the boy's genome is shared only by today's Native Americans and no other groups, showing a close relationship. Yet the child's Y chromosome belongs to a genetic group called Y haplogroup R, and its mitochondrial DNA to a haplogroup U. Today, those haplogroups are found almost exclusively in people living in Europe and regions of Asia west of the Altai Mountains, which are near the borders of Russia, China, and Mongolia.

One expected relationship was missing from the picture: The boy's genome showed no connection to modern East Asians. DNA studies of living people strongly suggest that East Asians—perhaps Siberians, Chinese, or Japanese—make up the major part of Native American ancestors (Balter, 2013).

These findings are consistent with earlier ones. Strong dental and cranial affinities exist between remains from the same site and those of Upper Paleolithic Europeans (Alexeyev and Gokhman, 1994). Also, when we compare the Clovis sites of early Amerindians (13,000 BP) with early European and Siberian sites (20,000-15,000 BP), we find many features in common: characteristic lithic technology, grave goods with red ocher, and sites with small shallow basins (Goebel, 1999; Haynes, 1980; Haynes, 1982).

What do these findings tell us? I would propose the following:

1. When the last ice age began some 25,000 years ago, a single population of nomadic hunters occupied the steppe-tundra that stretched from southwestern France to Beringia.

2. Ancestral East Asians had already split away from this proto-Eurasian population. They had probably adapted to life farther south in the more temperate environments of what is now north China. The Ainu may be an evolutionarily conservative branch of these East Asians.

3. At the height of the last ice age some 20,000 to 17,000 years ago, Siberia became virtually devoid of human life (Graf, 2009a; Graf, 2009b). Proto-Eurasians survived in refugia in parts of Europe to the west and in coastal regions of northeast Asia, Beringia and northwest North America to the east. Kennewick Man (c. 9,000-10,000 BP) may have been an example of this refuge population.

4. Siberia was then repeopled by two streams of settlement. One was composed of ‘Kennewickians’ spreading westward and inland from coastal refugia. The other stream was composed of early East Asians spreading northward.

5. This new mixed population of eastern Siberia and Beringia would later spread eastward into the interior of post-glacial North America around 13,000 years ago. These people were the early Amerindians of the Clovis culture.

It would be interesting to know what the reconstructed Mal’ta genome tells us about the skin, hair, and eye color of the proto-Eurasians. Were they pale-skinned with a diverse palette of hair and eye colors, like modern Europeans? Or were they brown-skinned with black hair and brown eyes, like modern Amerindians?  Probably the second possibility, given that the European color scheme seems to be a later evolutionary development—11,000 to 19,000 years ago for white skin and probably the same time frame for diversification of hair and eye color (Beleza et al., 2013). The Mal’ta people might have gone on to develop the same characteristics during this time frame, but they all died out at the height of the last ice age. 

In short, the Mal’ta people probably looked very much like native Indians with a more European skull shape, perhaps like the Ainu of northern Japan or the Kennewick humans of North America. 

References

Alexeyev, V.P., and I.I. Gokhman. (1994). Skeletal remains of infants from a burial on the Mal'ta Upper Paleolithic site, Homo, 45, 119‑126. 

Balter, M. (2013). Ancient DNA links Native Americans with Europe, Science, 342, 409-410.

http://www.sciencemag.org/content/342/6157/409.full

Beleza, S., A. Múrias dos Santos, B. McEvoy, I. Alves, C. Martinho, E. Cameron, M.D. Shriver, E.J. Parra, and J. Rocha. (2013). The timing of pigmentation lightening in Europeans, Molecular Biology and Evolution, 30, 24-35.

http://www.utm.utoronto.ca/~parraest/profile/PDF%20files/Beleza-2012(Mol.Biol.Evol.).pdf 

Goebel, T. (1999). Pleistocene human colonization of Siberia and peopling of the Americas: An ecological approach, Evolutionary Anthropology, 8, 208‑227.

http://onlinelibrary.wiley.com/doi/10.1002/(SICI)1520-6505(1999)8:6%3C208::AID-EVAN2%3E3.0.CO;2-M/abstract

Graf, K.E. (2009a). “The Good, the Bad, and the Ugly”: evaluating the radiocarbon chronology of the middle and late Upper Paleolithic in the Enisei River valley, south-central Siberia. Journal of Archaeological Science, 36, 694–707.

http://www.centerfirstamericans.com/cfsa-publications/Graf-JAS2009-36-694.pdf

Graf, K.E. (2009b). Modern human colonization of the Siberian Mammoth Steppe: A view from South-Central Siberia. In M. Camps, P. Chauhan (eds.), Sourcebook of Paleolithic transitions (pp. 484-496), Springer Science & Business Media.

Haynes, C.V. (1982). Were Clovis progenitors in Beringia? In D.M. Hopkins (ed). Paleoecology of Beringia, (pp. 383‑398), New York: Academic Press. 

Haynes, C.V. (1980). The Clovis culture, Canadian Journal of Anthropology, 1, 115‑121.

Is something afoot with Bigfoot?

 

Purported Yeti scalp at Khumjung Monastery (source). Has DNA been retrieved from it for the Oxford-Lausanne Collateral Hominid Project?

 

Over a year ago, geneticist Bryan Sykes launched the Oxford-Lausanne Collateral Hominid Project:

As part of a larger enquiry into the genetic relationship between our own species Homo sapiens and other hominids, we invite submissions of organic material from formally undescribed species, or “cryptids”, for the purpose of their species identification by genetic means. (Sykes, 2012)

The aim was to retrieve DNA from alleged remains of Yeti, Bigfoot, and the like. At the time, I was skeptical that anything would come of the project, since most remains of this type seem to be of dubious provenance. And then there’s the problem of contamination due to human handling.

So I was surprised to see this update on the project webpage, dated August 2013:

Thanks to all who have contributed samples to the project. We have collected and analysed over thirty samples and results are being prepared for publication. Following normal procedure, no results or other information will be available prior to publication, so please do not enquire.

Academics normally don’t like to publish negative results. When I googled the project name, I came across this report about Bryan Sykes meeting with people who had submitted samples of alleged Bigfoot remains: 

Interestingly, Professor Sykes has been visiting North America recently in order to speak with some of the researchers who have submitted samples, and he has also met with US Fish and Wildlife officials at one of their main laboratories located in Melford, Oregon. It has been revealed that Professor Sykes was in California very recently to speak with Justin Smeja, and also to be filmed for a documentary detailing his study which will be released on BBC Channel 4 once the results of the many samples tested by Sykes are published in a scientific journal. (Cooney, 2013)

Something seems to be afoot.  

References

Cooney, J. (2013). Exciting updates on the Oxford-Lausanne Collateral Hominid Project, Bizarre Zoology, June 12

http://bizarrezoology.blogspot.ca/2013/06/exciting-updates-on-oxford-lausanne.html

Sykes, B. (2012). Oxford-Lausanne Collateral Hominid Project, Wolfson College, University of Oxford

https://www.wolfson.ox.ac.uk/academic/GBFs-v/OLCHP

When was the split?

Genetic data suggest that ancestral East Asians diverged from ancestral Europeans long after the African/non-African split (source). This timeline, however, seems to be challenged by archaic DNA that is reputed to be 40,000 years old.

 

When did the ancestors of Europeans and East Asians part company? In my opinion, the divergence must have happened long after the time (c. 50,000 BP) when modern humans began to spread out of Africa. It probably occurred near the onset of the last ice age (25,000 – 10,000 BP), when advancing ice sheets and glacial lakes restricted gene flow between the western and eastern ends of Eurasia (Rogers, 1986).

This timeline is supported by several pieces of evidence:

1. Human skin began to lighten some 30,000 years ago in a population that was ancestral to both Europeans and East Asians (Beleza et al., 2012). A second phase of skin lightening, which affected only Europeans, occurred between 19,000 and 13,000 years ago. Proto-Eurasians must have therefore begun to diverge into two groups somewhere between 30,000 BP and 19,000 BP.

2. A Y-chromosome study suggests that all North Eurasian peoples descend from a common ancestral population dated to about 15,000 BP (Stepanov & Puzyrev, 2000; see also Armour et al., 1996; Santos et al., 1999; Zerjal et al., 1997).

3. The language families of northern Eurasia, particularly Uralic and Yukaghir and more generally Uralic-Yukaghir, Eskimo-Aleut, Chukotko-Kamchatkan and Altaic, share deep structural affinities that point to a common origin and not simply to word borrowing (Cavalli-Sforza, 1994, pp. 97-99; Fortescue, 1998; Rogers, 1986).

4. Archeological evidence (characteristic lithic technology, grave goods with red ocher, and sites with small shallow basins) shows the presence of a common cultural tradition throughout Europe and Siberia 20,000 to 15,000 years ago (Goebel, 1999; Haynes, 1980; Haynes, 1982).

5. Dental and cranial remains from Mal’ta (23,000-20,000 BP) in southern Siberia indicate strong affinities with Upper Paleolithic Europeans (Alexeyev & Gokhman, 1994; Goebel, 1999).

Back to the drawing board?

Nonetheless, this timeline now seems disproved by a recent study of archaic DNA:

We have extracted DNA from a 40,000-y-old anatomically modern human from Tianyuan Cave outside Beijing, China. […] The nuclear DNA sequences determined from this early modern human reveal that the Tianyuan individual derived from a population that was ancestral to many present-day Asians and Native Americans but postdated the divergence of Asians from Europeans. (Fu et al., 2013)

So ancestral Europeans and East Asians had already begun to diverge from each other by 40,000 BP. Considering that modern humans entered the Middle East around 46-47,000 BP, the time of divergence must have been close to the initial split between Africans and non-Africans (Schwarcz et al., 1979). Yet the genetic data argue otherwise.

When a new finding seems inconsistent with other data, one should take a second look. Do those human remains from Tianyuan Cave really date back to 40,000 years ago? Actually, they were initially dated to 25,000 BP, by means of uranium series dating of deer teeth from the same cave layer (Tong et al., 2004). Because this dating method is considered problematic when applied to organic remains, radiocarbon dating was later used to get a firmer date, which turned out to be 39,000 – 42,000 BP (Shang et al., 2007).

The two dating methods differed by 15,000 years. That’s a big discrepancy, and it may be why Shang et al. (2007) repeated their radiocarbon dating on several organic remains from the same layer. Such an approach, however, doesn’t rule out the possibility of a shared source of error, either in the remains themselves or in the testing laboratory.

There are two other reasons for doubting the estimate of 40,000 BP:

Associated faunal remains

The modern human remains from layer III were associated with the remains of other fauna. In general, the faunal assemblage indicates a significantly colder climate than the one that now prevails around Beijing. On the one hand, layer III had remains of the Siberian musk deer (Moschus moschiferus), which now lives farther north in the taiga of southern Siberia and northern Manchuria. On the other hand, layer III had no remains of warm climate species, i.e., the rhesus macaque (Macaca mulatta) and the masked palm civet (Paguma larvata), even though these species were present in the uppermost Holocene layer (Shang et al., 2007). The faunal evidence is thus consistent with the colder climate that existed when the last ice age began 25,000 years ago. It is not consistent with the warmer climate that prevailed 40,000 years ago in southern Siberia and northern China during the Malokheta Interstade of the Karga Interglacial (33,000 - 43,000 BP). At that time, average annual temperatures were as much as 2-3° C warmer than they are today (Goebel, 2004).

An outlier among finds of early East Asians

With a dating of 40,000 BP, these remains are much older than all other known finds that might be ancestral to present-day East Asians. The oldest rivals to Tianyuan Cave are Yamashita-cho, Okinawa (≈32,000 BP), Zhoukoudian Upper Cave, China (24,000 – 29,000 BP), Pinza-Abu, Okinawa ( ≈26,000 BP), and Minatogawa, Okinawa (≈18,000 BP) (Shang et al., 2007).

Conclusion

Archaic DNA promises to revolutionize our understanding of human origins. Unfortunately, it may also confer an aura of false certainty on new findings, thereby discouraging the healthy skepticism that makes good science possible. The Tianyuan Cave remains are undoubtedly those of an early East Asian and thus promise to shed much light on the beginnings of this branch of humanity. There are, however, reasons for doubting the date of 40,000 BP, and such doubts will probably become more insistent as we retrieve archaic DNA from other East Asian remains.

References

Alexeyev, V.P., & I.I. Gokhman. (1994). Skeletal remains of infants from a burial on the Mal'ta Upper Paleolithic site, Homo, 45, 119‑126.

Armour, J.A.L., T. Anttinen, C.A. May, E.E. Vega, A. Sajantila, J.R. Kidd, K.K. Kidd, J. Bertranpetit, S. Paabo, A.J. & Jeffreys. (1996). Minisatellite diversity supports a recent African origin for modern humans, Nature Genetics, 13, 154‑160.

Beleza, S., A. Múrias dos Santos, B. McEvoy, I. Alves, C. Martinho, E. Cameron, M.D. Shriver, E.J. Parra, & J. Rocha. (2012). The timing of pigmentation lightening in Europeans, Molecular Biology and Evolution, 20, online

Cavalli-Sforza, L.L., P. Menozzi, & A. Piazza. (1994). The History and Geography of Human Genes, Princeton: Princeton University Press.

Fortescue, M.D. (1998). Language Relations across Bering Strait. Reappraising the Archaeological and Linguistic Evidence, Cassell: London.

Fu, Q., M. Meyer, X. Gao, U. Stenzel, H. A. Burbano, J. Kelso, & S. Pääbo. (2013). DNA analysis of an early modern human from Tianyuan Cave, China, Proceedings of the National Academy of Sciences U.S.A., published ahead of print January 22, 2013, doi:10.1073/pnas.1221359110

http://intl.pnas.org/content/early/2013/01/17/1221359110.abstract

Goebel, T. (2004) “The early Upper Paleolithic of Siberia” (pp. 162-195) in S.L. Kuhn, K.W. Kerry (eds). The Early Upper Paleolithic beyond Western Europe, University of California Press.

Goebel, T. (1999). Pleistocene human colonization of Siberia and peopling of the Americas: An ecological approach, Evolutionary Anthropology, 8, 208‑227.

Haynes, C.V. (1982). Were Clovis progenitors in Beringia? In D.M. Hopkins (ed). Paleoecology of Beringia, New York: Academic Press, pp. 383‑398.

Haynes, C.V. (1980). The Clovis culture, Canadian Journal of Anthropology, 1, 115‑121.

Rogers, R.A. (1986). Language, human subspeciation, and Ice Age barriers in Northern Siberia, Canadian Journal of Anthropology, 5, 11‑22. 

Santos, F.R., A. Pandya, C. Tyler‑Smith, S.D.J. Pena, M. Schanfield, W.R. Leonard, L. Osipova, M.H. Crawford, & R.J. Mitchell. (1999). The Central Siberian origin for Native American Y chromosomes, American Journal of Human Genetics, 64, 619‑628.

Schwarcz, H.P., B. Blackwell, P. Goldberg, & A.E. Marks. (1979). Uranium series dating of travertine from archaeological sites, Nahal Zin, Israel, Nature, 277, 558-560.

Shang, H., H. Tong, S. Zhang, F. Chen, & E. Trinkaus. (2007). An early modern human from Tianyuan Cave, Zhoukoudian, China, Proceedings of the National Academy of Sciences U.S.A., 104, 6573-6578.

http://www.pnas.org/content/104/16/6573.full

Stepanov, V.A., & V.P. Puzyrev. (2000). Evolution of Y‑chromosome haplotypes in populations of North Eurasia, American Journal of Human Genetics, 67, 220.

Tong, H., H. Shang, S. Zhang, & F. Chen. (2004). A preliminary report on the newly found Tianyuan Cave, a Late Pleistocene human fossil site near Zhoukoudian, Chinese Science Bulletin, 49, 853-857.

http://link.springer.com/article/10.1007%2FBF02889760?LI=true

Zerjal, T., B. Dashnyam, A. Pandya, M. Kayser, L. Roewer, F.R. Santos, W. Scheifenhövel, N. Fretwell, M.A. Jobling, S. Harihara, K. Shimizu, D. Semjidmaa, A. Sajantila, P. Salo, M.H. Crawford, E.K. Ginter, O.V. Evgrafov, & C. Tyler‑Smith. (1997). Genetic relationships of Asians and Northern Europeans, revealed by Y‑chromosomal DNA analysis, American Journal of Human Genetics, 60, 1174‑1183.