Culture creates genetic structure in the Caucasus: Autosomal, mitochondrial, and Y-chromosomal variation in Daghestan

1471-2156-9-47 1471-2156 Research article Culture creates genetic structure in the Caucasus: Autosomal, mitochondrial, and Y-chromosomal variation in Daghestan Marchani E Elizabeth liz.marchani@anthro.utah.edu Watkins W Scott swatkins@genetics.utah.edu Bulayeva Kazima culikan@yahoo.com Harpending C Henry harpend@xmission.com Jorde B Lynn lbj@genetics.utah.edu

Department of Anthropology, University of Utah, Salt Lake City, UT 84112, USA

Eccles Institute of Human Genetics, University of Utah, Salt Lake City, UT 84112, USA

N.I. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow 117991, Russia

BMC Genetics 1471-2156 2008 9 1 47 http://www.biomedcentral.com/1471-2156/9/47 18637195 10.1186/1471-2156-9-47 25 1 2008 17 7 2008 17 7 2008 2008 Marchani et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

Near the junction of three major continents, the Caucasus region has been an important thoroughfare for human migration. While the Caucasus Mountains have diverted human traffic to the few lowland regions that provide a gateway from north to south between the Caspian and Black Seas, highland populations have been isolated by their remote geographic location and their practice of patrilocal endogamy. We investigate how these cultural and historical differences between highland and lowland populations have affected patterns of genetic diversity. We test 1) whether the highland practice of patrilocal endogamy has generated sex-specific population relationships, and 2) whether the history of migration and military conquest associated with the lowland populations has left Central Asian genes in the Caucasus, by comparing genetic diversity and pairwise population relationships between Daghestani populations and reference populations throughout Europe and Asia for autosomal, mitochondrial, and Y-chromosomal markers.

Results

We found that the highland Daghestani populations had contrasting histories for the mitochondrial DNA and Y-chromosome data sets. Y-chromosomal haplogroup diversity was reduced among highland Daghestani populations when compared to other populations and to highland Daghestani mitochondrial DNA haplogroup diversity. Lowland Daghestani populations showed Turkish and Central Asian affinities for both mitochondrial and Y-chromosomal data sets. Autosomal population histories are strongly correlated to the pattern observed for the mitochondrial DNA data set, while the correlation between the mitochondrial DNA and Y-chromosome distance matrices was weak and not significant.

Conclusion

The reduced Y-chromosomal diversity exhibited by highland Daghestani populations is consistent with genetic drift caused by patrilocal endogamy. Mitochondrial and Y-chromosomal phylogeographic comparisons indicate a common Near Eastern origin of highland populations. Lowland Daghestani populations show varying influence from Near Eastern and Central Asian populations.

Background

The populations of the Caucasus region have complex histories of isolation and gene flow. The region as a whole has served as a gateway between continents, with waves of human migration leaving rich cultural and linguistic diversity in their wake 12. The Caucasus Mountains have shaped the routes of migrating populations and military invasions, diverting these travellers away from the remote highlands and into the more easily accessible lowlands. Differences between highland and lowland populations are exaggerated by the marriage practices of highland populations: wives move to the home of their husbands, while husbands remain in the land of their forefathers for generations 34.

We have identified five populations from Daghestan that have been influenced by both physical and cultural barriers to gene flow. Three are highland isolates, while two lowland populations represent admixed groups influenced by Turkic and Mongolian migrants. We investigate whether the geographic barrier of altitude, the cultural barrier of patrilocal endogamy, or the introduction of migrants from a great distance have left detectable patterns in the genetic diversity of these populations. Specifically, we ask 1) whether geographic isolation and patrilocal endogamy have caused more genetic drift in highland than lowland populations, and 2) whether lowland populations show evidence of admixture from Turkic and Mongolian migrants.

We test these hypotheses by comparing mitochondrial DNA (mtDNA) and Y-chromosome (non-recombining, NRY) haplogroup frequencies among Daghestani, Near Eastern, Central Asian, Central/Northern European, and East Asian populations, as well as autosomal variation in 100 polymorphic Alu insertions among Daghestani, Central/Northern European, and East Asian populations. We compare measures of haplogroup diversity and pairwise distance for the mtDNA and NRY markers, then compare these to genetic distances from the autosomal data, looking for evidence of genetic drift and shared origins. Our results demonstrate that the cultural practice of patrilocality and historic population movements have shaped genetic variation in these Caucasus populations.

Methods

Populations

The Avar, Dargin, and Kubachi populations sampled in our study live in the highlands of Daghestan (Figure 1). They each speak different languages belonging to the Northeast Caucasian language family. The Avars and Dargins have traditionally been agriculturalists and pastoralists, while the Kubachi have specialized in jewelry making 5. These highland populations are isolated due to their remote location, their linguistic variation, and their practice of strict patrilocal endogamy 34. This marriage practice controls the inheritance of property and restricts male gene flow 3. These populations are thought to be indigenous to the region but, like other native peoples of the Caucasus region, their exact origins are unclear 6. Previous genetic studies have revealed that populations within the Caucasus region do not share the genetic variation believed by some researchers to be a signature of the Neolithic expansion through Europe, leading some to infer that these populations are remnants of a more ancient Eurasian population 378. Others suggest that the Caucasus region is instead inhabited by a collection of peoples who represent those who have travelled through or invaded the region in the historic past 4910.

Figure 1

Map of Population Sample Locations

Map of Population Sample Locations. This simplified and stylized map illustrates the location associated with each population sampled. Central/Northern European and East Asian samples are as described in the Methods section.

The Nogai and Kumiks of the Daghestani lowlands have a history of admixture. These populations speak different languages belonging to the Kipchak division of the Turkic language family and are more exogamous than the highland populations 1112. The Kumik population represents a mixture of native peoples of the Caucasus with Turkic migrants from the 4^thto the 15^thcenturies and may be descended from the Kipchaks, an ancient Turkic population 1012. The Kumiks currently practice a flexible form of virilocality and frequently exchange mates with other villages. The Nogai are descended from the Nogai khanate of the Mongol empire, established in the 12^thcentury, which arrived in Daghestan in the 13^thand 14^thcenturies 511. Although administrated by Mongolians, this khanate was peopled by many native Caucasian ethnic groups 1112, suggesting that the Nogai are an admixed population. The Nogai practice dual exogamy, prohibiting marriage within one's kin group or patronymic, a practice that encourages gene flow.

Overall, the five ethnic groups sampled for our study are representative of the genetic variation to be found in Daghestan, as these groups represent approximately one-half of the country's population 3. DNA samples were obtained following voluntary consent procedures developed and approved by the Daghestan IRB at the Institute of History, Archeology and Ethnology of Daghestan Center, of the Russian Academy of Sciences.

To place the genetic variation observed within Daghestan into a regional perspective, we include mtDNA and NRY data obtained from the literature for several Near Eastern and Central Asian populations in our analyses. Near Eastern populations include Crimean Tatars 213, Georgians 214, Iranians 213, and Turks 1415. The Central Asian populations included in this study are Kazak 213, Karakalpak 213, and Mongolian 216.

We are unable to include these Near Eastern and Central Asian population in our analyses of autosomal Alu insertion variation, as comparable data have not been published. We therefore include Central/Northern European and East Asian populations in our study of mtDNA, NRY, and Alu insertion variation. Our Central/Northern European sample includes 15 French and 57 Utahns of Central/Northern European ancestry, while the East Asian population includes 9 Cambodians, 13 Han Chinese, 16 Japanese, 5 Malay, 3 Taiwanese, and 9 Vietnamese individuals. These populations are geographically and genetically more distant from the Daghestani populations than the Near Eastern and Central Asian populations. As such, they act as extreme values in pairwise distance calculations and principal components analyses. These populations place the observed differences between Daghestani and other populations into a broader perspective. Distances between Daghestani populations and the Central/Northern European and East Asian populations serve as a yardstick against which distances within Daghestan, and between Daghestani populations and populations from the Near East and Central Asia may be measured.

Mitochondrial DNA Haplogroup Variation

We have genotyped 62 Avar, 28 Dargin, 25 Kubachi, 26 Kumik, 33 Nogai, 54 East Asian, and 71 Central/Northern European individuals for the following 24 mtDNA haplogroup-defining single nucleotide polymorphisms (SNPs) using ABI SNaPshot (Applied Biosystems, Foster City, CA) multiplexes designed by WSW 17: A1811G, T4646C, A4833G, C4883T, G7598A, A7768G, G7805A, A7933G, C8137T, G8994A, G9055A, T9090C, G9266A, A9545G, C10400T, T10436C, C10810T, C10873T, A12308G, A12612G, T12705C, A13263G, T14766C, A14793G. We have refined these data by identifying mtDNA haplogroup defining SNPs 16181920 in the HVS-I sequences of our samples. We performed new HVS-I sequencing for our Avar samples, while the sequences for the other Daghestani populations are available in the literature 3. We were able to define 26 mtDNA haplogroups with these data, with the combinations of SNPs used to define each mtDNA haplogroup in our samples listed in additional file 1: mtDNAdefinitions.xls. MtDNA haplogroup frequencies among Near Eastern and Central Asian populations were obtained from the literature 131416.

Additional file 1

Mitochondrial DNA Haplogroup Definitions. Describes how Daghestani, East Asian, and Central/Northern European samples were assigned to haplogroups.

Click here for file

Y-chromosome Haplogroup Variation

In a similar fashion, we have genotyped the males of the above sample (18 Avar, 8 Dargin, 14 Kubachi, 10 Kumik, 16 Nogai, 31 East Asian, and 61 Central/Northern European individuals) for the following 19 NRY haplogroup-defining SNPs using ABI SNaPshot (Applied Biosystems, Foster City, CA) multiplexes designed by WSW 17: M122, M145, M17, M170, M172, M173, M174, M175, M181, M20, M201, M207, M216, M52, M74, M89, M9, M91, M96. NRY haplogroup frequencies among Near Eastern and Central Asian populations were obtained from the literature 215. We follow the phylogeny and nomenclature established by the Y Chromosome Consortium 21, with the combination of SNPs used to define each haplogroup listed in additional file 2: NRYdefinitions.xls.

Additional file 2

Y-chromosome Haplogroup Definitions. Describes how Daghestani, East Asian, and Central/Northern European samples were assigned to haplogroups.

Click here for file

Autosomal Alu Insertion Variation

Genotypes for 100 Alu insertions have been previously published 22 for the Dargin, Kubachi, Kumik, Nogai, Central/Northern European and East Asian individuals genotyped for the mtDNA SNPs.

Analytical Methods

Haplogroup diversity within Daghestani populations was calculated using Nei's h statistic 23. The pairwise genetic distances between populations were calculated using population pairwise F_ST. Genetic distances were tested for significant differences from zero with 10,000 permutations in a randomization test (Arlequin 2.0; 24). Principal components analyses were performed using MATLAB R2007b in order to visualize the genetic relationships between populations. Mantel tests, using 10,000 random permutations in Arlequin 2.0, were performed to assess the correlations among the NRY, mtDNA, and Alu distance matrices.

Results

Haplogroup Frequencies and Diversity

Mitochondrial haplogroup frequencies and diversity values are presented in Table 1. The Daghestani populations resemble our samples from Central/Northern Europe and Turkey in their frequencies of common haplogroups HV, T, and U5. The highland Kubachi are an exception, with more than 75% of the sample possessing subtypes of haplogroup U, most commonly observed in Central/Northern Europe and Russia 25. The lowland Nogai samples resemble the samples from Central and East Asia, as all have appreciable frequencies of haplogroups B, C, and D. The range of haplogroup diversity values within Daghestan lies within the range observed among other populations, with neither highland (Avar, Dargin, Kubachi) nor lowland (Kumik, Nogai) Daghestani populations exhibiting unusually high or low values.

Table 1

Mitochondrial DNA Haplogroup Frequencies and Diversity.

Avar

Dargin

Kubachi

Kumik

Nogai

Crimean Tatar¹

Georgian²

Iranian¹

Turkish²

Karakalpak¹

Kazak¹

Mongolian³

N. Europe

East Asian

Sample Size

0.00

0.04

0.00

0.02

0.00

0.08

0.00

0.06

0.00

0.06

0.00

0.09

0.00

0.08

0.00

0.09

0.00

0.10

0.00

0.05

0.08

0.00

0.02

0.00

0.15

0.00

0.05

0.01

0.20

0.10

0.30

0.00

0.22

0.00

0.05

0.00

0.13

0.00

0.15

0.00

0.07

0.00

0.04

0.03

0.00

0.01

0.05

0.20

0.10

0.00

0.02

0.20

0.43

0.12

0.46

0.27

0.20

0.22

0.15

0.36

0.25

0.20

0.03

0.55

0.00

0.06

0.04

0.00

0.04

0.00

0.10

0.09

0.10

0.09

0.05

0.00

0.11

0.00

0.08

0.07

0.04

0.09

0.10

0.09

0.10

0.06

0.00

0.10

0.00

0.06

0.00

0.02

0.00

0.10

0.05

0.08

0.00

0.39

0.06

0.04

0.00

0.10

0.09

0.25

0.06

0.00

0.04

0.00

0.06

0.00

0.05

0.10

0.02

0.10

0.05

0.01

0.03

0.04

0.10

0.07

0.00

0.04

0.06

0.30

0.14

0.05

0.11

0.05

0.01

0.10

0.00

0.02

0.00

0.03

0.00

0.48

0.12

0.00

0.05

0.07

0.10

0.05

0.00

0.24

0.00

0.03

0.00

0.03

0.00

0.02

0.00

0.07

0.00

0.10

0.03

0.00

0.02

0.00

0.05

0.11

0.00

0.03

0.05

0.03

0.00

0.01

0.00

0.01

0.00

0.05

0.07

0.04

0.08

0.03

0.00

0.02

0.05

0.06

0.00

0.10

0.03

0.07

0.00

0.02

0.00

0.23

0.00

0.15

0.00

0.05

0.00

0.01

0.00

0.03

0.00

0.15

0.00

0.04

0.00

0.09

0.00

0.03

0.00

0.05

0.00

0.09

0.00

0.05

0.02

0.00

0.04

Nei's h

0.84

0.75

0.66

0.71

0.84

0.78

0.87

0.82

0.83

0.81

0.84

0.85

0.65

0.75

Haplogroups as defined in Additional File 1. Superscripts refer to the reference number of the source data.

References: 1. Comas et al. (2004); 2. Quintana-Murci et al. (2004); 3. Yao et al. (2004)

NRY haplogroup frequencies and diversity values are presented in Table 2. The highland Avar, Dargin, and Kubachi populations exhibit high frequencies of haplogroup F (including haplogroup G, see Discussion), which is also common in many Near Eastern populations. The lowland Nogai and Kumik samples exhibit a mixture of European, Near Eastern, and Central Asian haplogroups. The lowland Kumik and Nogai populations have NRY haplogroup diversity values as high as those observed in the Near East and Central Asia, while the highland Daghestani populations have lower NRY haplogroup diversity, less than or equal to that observed in our Central/Northern European sample. The highland Dargins are exceptional, with a Nei's h value of zero, as all males sampled belong to NRY haplogroup F.

Table 2

Y-Chromosome Haplogroup Frequencies and Diversity.

Avar

Dargin

Kubachi

Kumik

Nogai

Crimean Tatar¹

Georgian²

Iranian¹

Turkish²

Karakalpak¹

Kazak¹

Mongolian³

C/N Europe

East Asian

Sample Size

523

0.00

0.13

0.09

0.00

0.01

0.22

0.66

0.59

0.00

0.03

0.00

0.06

0.05

0.04

0.19

0.00

0.03

0.00

0.11

0.00

0.02

0.04

0.00

F (F*xH,I,J2)

0.61

1.00

0.92

0.30

0.06

0.18

0.50

0.40

0.20

0.09

0.02

0.08

0.02

0.00

0.20

0.00

0.01

0.00

0.05

0.02

0.00

0.05

0.00

0.36

0.00

0.33

0.00

0.10

0.06

0.14

0.33

0.23

0.24

0.09

0.00

K (K*xL,O)

0.00

0.20

0.25

0.00

0.02

0.06

0.09

0.02

0.13

0.00

0.03

0.00

0.04

0.05

0.00

O (O*xO3)

0.00

0.06

0.05

0.00

0.02

0.04

0.00

0.39

0.00

0.05

0.00

0.02

0.00

0.11

0.09

0.08

0.00

0.52

P (P*x R1)

0.00

0.06

0.03

0.07

0.00

0.02

0.00

R1*

0.06

0.00

0.08

0.20

0.25

0.09

0.06

0.02

0.16

0.09

0.06

0.00

0.56

0.00

R1a1

0.00

0.13

0.32

0.06

0.02

0.07

0.18

0.04

0.05

0.00

Nei's h

0.48

0.00

0.14

0.70

0.78

0.79

0.63

0.72

0.85

0.84

0.53

0.60

0.55

0.56

Haplogroups as defined in Additional File 2. Superscripts refer to the reference number of the source data.

References: 1. Wells et al.(2001); 2. Cinnioglu et al.(2004); The symbol "x" means "excluding the following subtypes."

Haplogroups G, H, J (J*xJ2) have been genotyped for our Daghestani, Central/Northern European, and East Asian samples, though they are unavailable for the reference populations. Because of this, haplogroup F includes individuals who may belong to haplogroups G or J (xJ2).

Population Pairwise Distances

Genetic distances based on mtDNA haplogroup frequencies are shown in the upper triangle of Table 3, while the NRY pairwise distances are shown in the lower triangle. The NRY population pairwise distances show no differentiation between the highland Daghestani populations, while the Avar and Dargin highland populations are significantly different from the highland Kubachi with respect to the mtDNA. This suggests that either the history of Daghestani Y chromosomes differs from that of the mtDNA and autosomal loci, or that the males genotyped for the NRY polymorphisms are not sufficiently representative of the population at large. The Kumik and Turkish populations have F_STvalues of zero, while the Nogai have low genetic distances to the Near Eastern and Central Asian populations, for both the mtDNA and NRY data sets.

Table 3

Mitochondrial DNA and Y-chromosome Pairwise F_STValues.

Avar

Dargin

Kubachi

Kumik

Nogai

Crimean Tatar

Georgian

Iranian

Turkish

Karakalpak

Kazak

Mongolian

C/N European

East Asian

Avar

0.07

0.19

0.04

0.12

0.06

0.02

0.05

0.06

0.12

0.27

0.16

0.33

Dargin

0.14

0.20

0.00

0.08

0.01

0.02

0.05

0.00

0.10

0.11

0.30

0.02

0.38

Kubachi

0.14

0.00

0.20

0.25

0.20

0.18

0.24

0.19

0.29

0.27

0.43

0.34

0.51

Kumik

0.11

0.13

0.06

0.09

0.05

0.02

0.06

0.00

0.09

0.11

0.30

0.04

0.39

Nogai

0.25

0.24

0.20

0.02

0.10

0.09

0.02

0.10

0.00

0.08

0.17

0.12

Crimean Tatar

0.19

0.17

0.15

0.04

0.00

0.03

0.00

0.12

0.13

0.31

0.08

0.40

Georgian

0.00

0.07

0.06

0.20

0.16

0.01

0.00

0.10

0.11

0.27

0.08

0.34

Iranian

0.03

0.05

0.06

0.05

0.16

0.15

0.03

0.04

0.02

0.15

0.13

0.23

Turkish

0.05

0.08

0.06

0.00

0.05

0.06

0.04

0.06

0.10

0.13

0.30

0.03

0.36

Karakalpak

0.18

0.15

0.13

0.03

0.00

0.16

0.14

0.06

0.00

0.07

0.19

0.11

Kazak

0.36

0.31

0.31

0.28

0.23

0.26

0.33

0.27

0.24

0.16

0.05

0.22

0.09

Mongolian

0.34

0.29

0.30

0.25

0.21

0.22

0.30

0.22

0.21

0.13

0.00

0.39

0.00

C/N European

0.39

0.38

0.33

0.18

0.09

0.12

0.34

0.33

0.17

0.14

0.42

0.43