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Genetic data from Y chromosome STR and SNP loci in Ukrainian population

  • Marta Mielnik-Sikorska
    Affiliations
    Institute of Forensic Medicine, Department of Molecular and Forensic Genetics, Collegium Medicum of the Nicolaus Copernicus University, Marii Skłodowskiej-Curie Street 9, 85-094 Bydgoszcz, Poland
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  • Author Footnotes
    1 Current address: Institute of Human Genetics, Polish Academy of Sciences, Strzeszynska Street 32, 60-479 Poznań, Poland.
    Patrycja Daca
    Footnotes
    1 Current address: Institute of Human Genetics, Polish Academy of Sciences, Strzeszynska Street 32, 60-479 Poznań, Poland.
    Affiliations
    Institute of Forensic Medicine, Department of Molecular and Forensic Genetics, Collegium Medicum of the Nicolaus Copernicus University, Marii Skłodowskiej-Curie Street 9, 85-094 Bydgoszcz, Poland
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  • Marcin Woźniak
    Affiliations
    Institute of Forensic Medicine, Department of Molecular and Forensic Genetics, Collegium Medicum of the Nicolaus Copernicus University, Marii Skłodowskiej-Curie Street 9, 85-094 Bydgoszcz, Poland
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  • Boris A. Malyarchuk
    Affiliations
    Institute of Biological Problems of the North, Russian Academy of Sciences, Portovaya Street 18, 685-000 Magadan, Russia
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  • Jarosław Bednarek
    Affiliations
    Institute of Forensic Medicine, Department of Molecular and Forensic Genetics, Collegium Medicum of the Nicolaus Copernicus University, Marii Skłodowskiej-Curie Street 9, 85-094 Bydgoszcz, Poland
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  • Tadeusz Dobosz
    Affiliations
    Department of Forensic Medicine, Wrocław Medical University, Marii Skłodowskiej-Curie Street 52, 50-369 Wrocław, Poland
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  • Tomasz Grzybowski
    Correspondence
    Corresponding author.
    Affiliations
    Institute of Forensic Medicine, Department of Molecular and Forensic Genetics, Collegium Medicum of the Nicolaus Copernicus University, Marii Skłodowskiej-Curie Street 9, 85-094 Bydgoszcz, Poland
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  • Author Footnotes
    1 Current address: Institute of Human Genetics, Polish Academy of Sciences, Strzeszynska Street 32, 60-479 Poznań, Poland.

      Abstract

      We have tested a sample of 154 unrelated males from Lviv region (Ukraine) for 11 Y-chromosomal single nucleotide polymorphisms (SNPs) and 17 Y-chromosomal STR loci (DYS19, DYS385a, DYS385b, DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393, DYS437, DYS438, DYS439, DYS448, DYS456, DYS458, DYS635, YGATA_H4.1). Haplotype and haplogroup diversity values were calculated for the population under study. Genetic distances (RST) to 9 other Slavic populations were calculated based on 12 Y-STR loci. Haplotype frequencies and MDS plots were constructed based on genetic distances. Haplogroup frequency patterns revealed in Ukraine are similar to those characteristic of other European populations. However, it also allowed for identification a specific genetic component in Ukrainian sample which seems to originate from areas dwelled by Western Slavs, i.e. subhaplogroup R1a1a7, at frequency of 13.65%. Analysis of RST distances and AMOVA revealed high level of heterogeneity between Slavic populations inhabiting the south and north part of Europe, determined geographically rather than by linguistic factors. It has also been found a closer similarity (in the values of RST) between Ukrainian and Slovak populations than between Ukrainians and other Slavic population samples.

      Keywords

      1. Population

      Dried blood samples on paper were collected from 154 unrelated males from Lviv region (western part of Ukraine). The permission to perform this study was granted by the Bioethics Committee at the Collegium Medicum of the Nicolaus Copernicus University, Bydgoszcz, Poland (approval no. KB 466/2010).

      2. DNA extraction

      Total genomic DNA was extracted from blood samples by means of cell lysis in the presence of proteinase K and 2% SDS, followed by standard phenol/chlorophorm extraction.

      3. PCR and typing

      3.1 Y-STR analysis

      Samples were amplified using AmpFlSTR Yfiler™ kit including 17 loci (DYS19, DYS385a, DYS385b, DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393, DYS437, DYS438, DYS439, DYS448, DYS456, DYS458, DYS635, YGATA_H4.1) (Applied Biosystems) according to manufacturer's recommendations. Alleles were separated and detected using ABI 3130 capillary sequencer (Applied Biosystems). Haplotyping was performed using GeneMapper ID v.3.2 software (Applied Biosystems) according to manufacturer's recommendations. Alleles were named according to the published nomenclature and the updated ISFG guidelines for Y-STRs [
      • Gusmao L.
      • Butler J.M.
      • Carracedo A.
      • Gill P.
      • Kayser M.
      • Mayr W.R.
      • Morling N.
      • Prinz M.
      • Roewer L.
      • Tyler-Smith C.
      • Schneider P.M.
      DNA Commission of the International Society of Forensic Genetics (ISFG): an update of the recommendations on the use of Y-STRs in forensic analysis.
      ].

      3.2 Y-SNP analysis

      Haplogroup affinity was tested using selected SNP markers that are characteristic of major Eurasian haplogroups and subhaplogroups. The SNP markers used in the study are as follows: M9, M17, M35, M45, M89, M170, M172, M269, M458, P25, SRY10831.2. The SNP markers were assayed by SNaPshot analysis. Amplification of 11 Y-SNPs in two multiplex PCRs (MY-1, MY-R1) and subsequent single base extension were carried out according to Onofri et al. [
      • Onofri V.
      • Alessandrini F.
      • Turchi C.
      • Pesaresi M.
      • Buscemi L.
      • Tagliabracci A.
      Development of multiplex PCRs for evolutionary and forensic applications of 37 human Y chromosome SNPs.
      ]. Additionally we extend the MY-R1 multiplex with a new SNP marker M458 (which is common for Slavic population) based on Underhill et al. study [
      • Underhill P.A.
      • Myres N.M.
      • Rootsi S.
      • Metspalu M.
      • Zhivotovsky L.A.
      • King R.J.
      • Lin A.A.
      • Chow C.E.
      • Semino O.
      • Battaglia V.
      • Kutuev I.
      • Järve M.
      • Chaubey G.
      • Ayub Q.
      • Mohyuddin A.
      • Mehdi S.Q.
      • Sengupta S.
      • Rogaev E.I.
      • Khusnutdinova E.K.
      • Pshenichnov A.
      • Balanovsky O.
      • Balanovska E.
      • Jeran N.
      • Augustin D.H.
      • Baldovic M.
      • Herrera R.J.
      • Thangaraj K.
      • Singh V.
      • Singh L.
      • Majumder P.
      • Rudan P.
      • Primorac D.
      • Villems R.
      • Kivisild T.
      Separating the post-Glacial coancestry of European and Asian Y chromosomes within haplogroup R1a.
      ]. Detection of SNaPshot products and genotyping were carried out on the ABI 3130 capillary sequencer (Applied Biosystems) using the GeneMapper ID v3.2 software (Applied Biosystems). The Y-SNP haplogroup nomenclature used here complies with the recommendations of the Y Chromosome Consortium [
      • Karafet T.M.
      • Mendez F.L.
      • Meilerman M.B.
      • Underhill P.A.
      • Zegura S.L.
      • Hammer M.F.
      New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree.
      ].

      4. Statistical analysis

      Arlequin software version 3.1 [
      • Excoffier L.
      • Laval G.
      • Schneider S.
      Arlequin (version 3.0): an integrated software package for population genetics data analysis.
      ] was used to calculate allele and haplotype frequencies, gene diversities, haplotype diversity, RST distances and AMOVA. The statistical significance tests for RST were performed at 1000 permutations and for AMOVA at 20 000 permutations. Our population data were compared with the previously described neighboring European populations belonging to Slavic speaking group. These populations included Poland [
      • Rębała K.
      • Mikulich A.I.
      • Tsybovsky I.S.
      • Siváková D.
      • Dzupinková Z.
      • Szczerkowska-Dobosz A.
      • Szczerkowska Z.
      Y-STR variation among Slavs: evidence for the Slavic homeland in the middle Dnieper basin.
      ,
      • Woźniak M.
      • Grzybowski T.
      • Starzyński J.
      • Marciniak T.
      Continuity of Y chromosome haplotypes in the population of Southern Poland before and after the Second World War.
      ,
      • Woźniak M.
      • Malyarchuk B.
      • Derenko M.
      • Vanecek T.
      • Lazur J.
      • Gomolcak P.
      • Grzybowski T.
      Similarities and distinctions in Y chromosome gene pool of Western Slavs.
      ], Slovakia [
      • Woźniak M.
      • Malyarchuk B.
      • Derenko M.
      • Vanecek T.
      • Lazur J.
      • Gomolcak P.
      • Grzybowski T.
      Similarities and distinctions in Y chromosome gene pool of Western Slavs.
      ,
      • Rębała K.
      Analiza polimorfizmu 17 loci STR chromosomu Y metodą kompleksowej reakcji PCR.
      ], Czech Republic [
      • Woźniak M.
      • Malyarchuk B.
      • Derenko M.
      • Vanecek T.
      • Lazur J.
      • Gomolcak P.
      • Grzybowski T.
      Similarities and distinctions in Y chromosome gene pool of Western Slavs.
      ,
      • Zastera J.
      • Roewer L.
      • Willuweit S.
      • Sekerka P.
      • Benesova L.
      • Minarik M.
      Assembly of a large Y-STR haplotype database for the Czech population and investigation of its substructure.
      ], Croatia [
      • Ljubković J.
      • Stipisić A.
      • Sutlović D.
      • Definis-Gojanović M.
      • Bucan K.
      • Andelinović S.
      Y-chromosomal short tandem repeat haplotypes in southern Croatian male population defined by 17 loci.
      ,
      • Haliti N.
      • Carapina M.
      • Masić M.
      • Strinović D.
      • Klarić I.M.
      • Kubat M.
      Evaluation of population variation at 17 autosomal STR and 16 Y-STR haplotype loci in Croatians.
      ], Macedonia [
      • Spiroski M.
      • Arsov T.
      • Krüger C.
      • Willuweit S.
      • Roewer L.
      Y-chromosomal STR haplotypes in Macedonian population samples.
      ], Montenegro [
      • Mirabal S.
      • Varljen T.
      • Gayden T.
      • Regueiro M.
      • Vujovic S.
      • Popovic D.
      • Djuric M.
      • Stojkovic O.
      • Herrera R.J.
      Human Y-chromosome short tandem repeats: a tale of acculturation and migrations as mechanisms for the diffusion of agriculture in the Balkan Peninsula.
      ], Serbia [
      • Mirabal S.
      • Varljen T.
      • Gayden T.
      • Regueiro M.
      • Vujovic S.
      • Popovic D.
      • Djuric M.
      • Stojkovic O.
      • Herrera R.J.
      Human Y-chromosome short tandem repeats: a tale of acculturation and migrations as mechanisms for the diffusion of agriculture in the Balkan Peninsula.
      ,
      • Veselinovic I.S.
      • Zgonjanin D.M.
      • Maletin M.P.
      • Stojkovic O.
      • Djurendic-Brenesel M.
      • Vukovic R.M.
      • Tasic M.M.
      Allele frequencies and population data for 17 Y-chromosome STR loci in a Serbian population sample from Vojvodina province.
      ], Belorussia [
      • Rębała K.
      • Tsybovsky I.S.
      • Bogacheva A.V.
      • Kotova S.A.
      • Mikulich A.I.
      • Szczerkowska Z.
      Forensic analysis of polymorphism and regional stratification of Y-chromosomal microsatellites in Belarus.
      ] and Russia [
      • Roewer L.
      • Croucher P.J.
      • Willuweit S.
      • Lu T.T.
      • Kayser M.
      • Lessig R.
      • de Knijff P.
      • Jobling M.A.
      • Tyler-Smith C.
      • Krawczak M.
      Signature of recent historical events in the European Y-chromosomal STR haplotype distribution.
      ,
      • Derenko M.
      • Malyarchuk B.
      • Denisova G.A.
      • Woźniak M.
      • Dambueva I.
      • Dorzhu C.
      • Luzina F.
      • Miścicka-Śliwka D.
      • Zakharov I.
      Contrasting patterns of Y-chromosome variation in South Siberian populations from Baikal and Altai-Sayan regions.
      ,
      • Derenko M.
      • Malyarchuk B.
      • Denisova G.
      • Woźniak M.
      • Grzybowski T.
      • Dambueva I.
      • Zakharov I.
      Y-chromosome haplogroup N dispersals from south Siberia to Europe.
      ]. For those population samples data for twelve Y-STR loci were available (DYS19, DYS385a, DYS385b, DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393, DYS437, DYS438, DYS439). Genetic distances were obtained in the form of RST values and illustrated by creating a MDS plot using the software package STATISTICA v. 7.1 (StatSoft, Inc., Tulsa, USA).
      Because some Ukrainian populations that are only available from the YHRD 3.0 [

      YHRD 3.0 Y Chromosome Haplotype Reference Database, 2011, http://www.yhrd.org/ (Release 38 built at: 30 December 2011).

      ] have been studied by means of 9 Y-STR loci (DYS19, DYS385a, DYS385b, DYS389I, DYS389II, DYS390, DYS391, DYS392, DYS393), we have used an AMOVA tool of the YHRD to measure the genetic distance between populations (RST statistics).

      4.1 Quality control

      A quality control check was performed using the proficiency testing of the Y-STR Haplotyping Quality Assurance Exercise 2000 (YC000039). Haplotype data were submitted to YHRD and received the accession number YA003749.

      5. Results

      Allele frequency distribution and gene diversity values calculated for each locus are listed in Table 1. Pairwise RST values for the compared Slavic populations are presented in Table 2. Variations among the Ukrainian and other nine Slavic populations can be seen at the MDS plot (Fig. 1). Haplotype and haplogroup data of the Ukrainian population are given in Supplementary material, Table S1.
      Table 1Allele frequencies and gene diversity values at 17 AmpFlSTR Yfiler loci in population sample from Lviv, Ukraine.
      AlleleLoci
      DYS19DYS389IDYS389IIDYS390DYS391DYS392DYS393DYS437DYS438DYS439DYS448DYS456DYS458DYS635Y H4HaplotypeDYS385
      80.0069–90.149
      90.0650.0450.02610–130.052
      100.5520.4480.1880.00610–140.214
      110.3640.8640.4030.3380.37711–110.013
      120.1100.0190.0450.0520.1040.3120.44811–120.013
      130.0780.7400.0190.8640.1040.0390.16211–130.019
      140.1100.1490.0710.0650.5910.0190.0520.0060.00611–140.006
      150.3050.0190.2860.0060.4030.22111–150.071
      15/160.00611–170.006
      160.3960.1230.2990.33112–140.006
      170.1040.1880.28612–150.084
      180.0190.0190.1300–160.058
      18.20.00613–130.026
      190.1360.02613–140.006
      200.7340.03913–150.026
      210.0190.0780.11713–160.065
      220.0520.0190.14913–170.019
      230.1170.0060.55814–140.006
      240.3900.13614–150.039
      250.0060.39014–160.013
      260.03214–170.006
      2714–180.019
      280.09715–150.006
      290.24715–160.006
      300.36415–180.006
      310.20116–180.013
      320.07817–180.013
      330.00618–200.026
      18–180.006
      GD0.7220.4200.7560.6830.5620.2480.2480.5580.6280.7460.4390.7130.7470.6360.6350.750
      GD: gene diversity.
      Table 2RST calculation for 12 Y-STR loci available for 10 Slavic populations.
      1.2.3.4.5.6.7.8.9.10.
      1. Poland++++++++++++++++++++++++++
      2. Slovakia0.018+++++++++++++++++
      3. Czech Republic0.0190.005+++++++++++++++++++++
      4.Croatia0.1390.0670.096++++++++++++++++++
      5. Macedonia0.2420.1400.1700.048+++++++++
      6. Montenegro0.2580.1610.1930.0630.000+++++++++++
      7. Serbia0.2030.1140.1450.0250.0020.009+++++++++
      8. Russia0.0110.0100.0150.1090.2040.2180.167+++
      9. Ukraine0.0370.0060.0260.0350.1060.1250.0780.027++
      10. Belorussia0.0080.0100.0210.1050.2080.2180.1650.0020.021
      Above the diagonal RST P values are indicated as “−” P > 0.05; “+” 0.05 > P > 0.005; “++” 0.005 > P > 0.001; “+++” P < 0.001.
      Figure thumbnail gr1
      Fig. 1MDS plot based on RST values for 12 Y-STR haplotypes showing relationships among 10 Slavic populations. Stress value for two dimensional MDS is 0.000603.

      6. Other remarks

      Ukrainians speak a language of Eastern Slavic subgroup of the Slavic language group. Ukrainian population is relatively poorly studied as far as Y chromosome STR-polymorphism is regarded. Previous studies have employed mainly low resolution approaches, based on the analysis of 5-loci Y-STR haplotypes only [
      • Kravchenko S.A.
      • Slominskii P.A.
      • Bets L.A.
      • Stepanova A.V.
      • Mikulich A.I.
      • Limborskaia S.A.
      • Livshits L.A.
      Polymorphism of the STR-locus of Y chromosomes in Eastern Slavs in three populations from Belorussia, Russia and the Ukraine.
      ] or the minimal Y-STR haplotypes [

      YHRD 3.0 Y Chromosome Haplotype Reference Database, 2011, http://www.yhrd.org/ (Release 38 built at: 30 December 2011).

      ]. The main purpose of this study was to expand published Y chromosome genetic data from the Ukrainian population using the information from the new Y-SNP and Y-STR loci, as well to present some additional information about the Y-STR genetic relationships of Ukrainian populations with the populations from the neighboring Slavic peoples.
      In the 154 Ukrainian samples analyzed in the study, a total of 147 different Y-STR haplotypes were observed. 140 haplotypes (95.24%) were unique, while the remaining 7 haplotypes appeared twice. In one sample we found a duplicated allele at DYS19 locus. We have also found intermediate alleles at loci DYS385a and DYS448 in two samples. Haplotype and haplogroup diversity values in our sample were 0.9995 and 0.7947, respectively. The highest gene diversity was observed for the single locus marker DYS389II (H = 0.756) and for a two-locus system DYS385 (H = 0.750).
      Haplogroups that were shown to be present in Lviv population were (in the order of their relative frequency): R1a1/M17 (31.17%), I*/+M170 (28.57%), R1a1a7/+M458 (13.65%), E1b1b1/+M35 (7.79%), R1b1/+P25 (5.19%), F*/+M89 (4.54%), J2*/+M172 (3.25%), R1b1a2/+M269 (2.59%) and K*/+M9 (1.95%). The data indicated that Y chromosome haplogroup frequency patterns revealed in Ukraine are similar to those characteristic of other European populations [
      • Pericić M.
      • Lauc L.B.
      • Klarić I.M.
      • Rootsi S.
      • Janićijevic B.
      • Rudan I.
      • Terzic R.
      • Colak I.
      • Kvesić A.
      • Popović D.
      • Sijacki A.
      • Behluli I.
      • Dordevic D.
      • Efremovska L.
      • Bajec D.D.
      • Stefanović B.D.
      • Villems R.
      • Rudan P.
      High-resolution phylogenetic analysis of southeastern Europe traces major episodes of paternal gene flow among Slavic populations.
      ]. However, it also allowed for identification a specific genetic component in Ukrainian sample which seem to originate from areas dwelled by Western Slavs, i.e. subhaplogroup R1a1a7 [
      • Underhill P.A.
      • Myres N.M.
      • Rootsi S.
      • Metspalu M.
      • Zhivotovsky L.A.
      • King R.J.
      • Lin A.A.
      • Chow C.E.
      • Semino O.
      • Battaglia V.
      • Kutuev I.
      • Järve M.
      • Chaubey G.
      • Ayub Q.
      • Mohyuddin A.
      • Mehdi S.Q.
      • Sengupta S.
      • Rogaev E.I.
      • Khusnutdinova E.K.
      • Pshenichnov A.
      • Balanovsky O.
      • Balanovska E.
      • Jeran N.
      • Augustin D.H.
      • Baldovic M.
      • Herrera R.J.
      • Thangaraj K.
      • Singh V.
      • Singh L.
      • Majumder P.
      • Rudan P.
      • Primorac D.
      • Villems R.
      • Kivisild T.
      Separating the post-Glacial coancestry of European and Asian Y chromosomes within haplogroup R1a.
      ].
      To analyze similarities and differences between our Ukrainian sample and other Slavic populations, the analysis of pairwise interpopulation genetic distances RST was performed (Table 2). Calculations as illustrated with the MDS plot (Fig. 1) has shown high level of heterogeneity between Slavic populations inhabiting the south and north part of Europe. The results of molecular variance analysis (AMOVA) based on variability of 12 Y-STR loci in Slavic populations grouped according to geographical or linguistic criteria (Table 3) has shown that the observed heterogeneity between southern and northern Slavic populations is determined geographically rather than by linguistic factors.
      Table 3AMOVA calculation results with P-values (in parentheses) for 12 Y-STRs in 10 Slavic population samples.
      Grouping criteriaAnalysis of molecular variance (%)
      Among groupsAmong populations within groupsWithin populations
      A8.60

      (0.00000 ± 0.00000)
      91.40

      (0.00000 ± 0.00000)
      B8.91

      (0.00939 ± 0.00072)
      1.67

      (0.00000 ± 0.00000)
      89.42

      (0.00000 ± 0.00000)
      C14.74

      (0.00365 ± 0.00042)
      1.58

      (0.00000 ± 0.00000)
      83.68

      (0.00000 ± 0.00000)
      The calculations were performed for: A – all Slavic populations grouped together; B – Slavic populations grouped on the basis of linguistic criteria: Eastern Slavs (Russia, Ukraine, Belorussia), Western Slavs (Poland, Czech Republic, Slovakia) and Southern Slavs (Croatia, Serbia, Macedonia, Montenegro); C – Slavic populations grouped on the basis of geographical criteria: Slavic nations living at the central and eastern part of Europe (Russia, Ukraine, Belorussia, Poland, Czech Republic, Slovakia) and southern part of Europe (Croatia, Serbia, Macedonia, Montenegro).
      Comparing the results of this study to those described previously [
      • Rębała K.
      • Mikulich A.I.
      • Tsybovsky I.S.
      • Siváková D.
      • Dzupinková Z.
      • Szczerkowska-Dobosz A.
      • Szczerkowska Z.
      Y-STR variation among Slavs: evidence for the Slavic homeland in the middle Dnieper basin.
      ] it is interesting to note the position of Ukraine population on the MDS plot. In our study this position suggests closer similarity between Ukrainian and Slovak populations (non-significant RST value) than between Ukrainians and other Slavic population samples. Since Ukrainian sample studied here originated from western part of Ukraine, it is reasonable to analyze between-population relationships relaying on population samples from other parts of the country. Database YHRD contains information on 9-loci Y-STR haplotypes in four Ukrainian populations representing western (Lviv, Uzhgorod) and eastern (Kiev, Lugansk) parts of Ukraine. Therefore, using the YHRD AMOVA tool we have performed analysis of variability of 9 STR loci in 5 Ukrainian populations and 5 neighboring populations from Belarus (Ivanava) [
      • Rębała K.
      • Tsybovsky I.S.
      • Bogacheva A.V.
      • Kotova S.A.
      • Mikulich A.I.
      • Szczerkowska Z.
      Forensic analysis of polymorphism and regional stratification of Y-chromosomal microsatellites in Belarus.
      ], Poland (Lublin) [
      • Ploski R.
      • Wozniak M.
      • Pawlowski R.
      • Monies D.M.
      • Branicki W.
      • Kupiec T.
      • Kloosterman A.
      • Dobosz T.
      • Bosch E.
      • Nowak M.
      • Lessig R.
      • Jobling M.A.
      • Roewer L.
      • Kayser M.
      Homogeneity and distinctiveness of Polish paternal lineages revealed by Y chromosome microsatellite haplotype analysis.
      ], Slovakia (Bratislava) [
      • Rębała K.
      • Mikulich A.I.
      • Tsybovsky I.S.
      • Siváková D.
      • Dzupinková Z.
      • Szczerkowska-Dobosz A.
      • Szczerkowska Z.
      Y-STR variation among Slavs: evidence for the Slavic homeland in the middle Dnieper basin.
      ], Czech Republic (Central Bohemia) [
      • Zastera J.
      • Roewer L.
      • Willuweit S.
      • Sekerka P.
      • Benesova L.
      • Minarik M.
      Assembly of a large Y-STR haplotype database for the Czech population and investigation of its substructure.
      ] and Russia (Orel) [
      • Roewer L.
      • Willuweit S.
      • Kruger C.
      • Nagy M.
      • Rychkov S.
      • Morozowa I.
      • Naumova O.
      • Schneider Y.
      • Zhukova O.
      • Stoneking M.
      • Nasidze I.
      Analysis of Y chromosome STR haplotypes in the European part of Russia reveals high diversities but non-significant genetic distances between populations.
      ]. As seen (Table 4), all but one (Uzhgorod) Ukrainian population as well as Slovaks are clustered together, showing the lowest values of RST statistics.
      Table 4RST calculation for 9 Y-STR loci available for 10 Slavic populations, including 5 Ukrainian samples.
      12345678910
      1. Bratislava (Slovakia)+++++++
      2. Central Bohemia (Czech Republic)0.018+++++++++++++++++++
      3. Ivanava (Belarus)0.0100.0449+++
      4. Kiev (Ukraine)−0.0030.03340.0074+++++++
      5. Lublin (Poland)0.0240.05830.00750.0198+++++++++++
      6. Lugansk (Ukraine)0.0020.0460.012−0.0030.017++++
      7. Lviv-1 (Ukraine)−0.0040.0180.0240.0020.0420.007++
      8. Orel (Russia)0.0170.0260.0020.0190.0120.0250.032++++++
      9. Uzhgorod (Ukraine)0.0230.0320.0730.0390.1040.0440.0070.082
      10. Lviv-2 (Ukraine)0.0050.0280.0410.0110.0560.018−0.0030.0520.002
      Above the diagonal RST P values are indicated as “−” P > 0.05; “+” 0.05 > P > 0.005; “++” 0.005 > P > 0.001; “+++” P < 0.001. Lviv-1 – YHRD data (Population ID YP000230); Lviv-2 – present study.
      These observations seem to challenge previous results obtained by Rębała et al. [
      • Rębała K.
      • Mikulich A.I.
      • Tsybovsky I.S.
      • Siváková D.
      • Dzupinková Z.
      • Szczerkowska-Dobosz A.
      • Szczerkowska Z.
      Y-STR variation among Slavs: evidence for the Slavic homeland in the middle Dnieper basin.
      ], where Ukrainian sample was indistinguishable in terms of FST distances from Russian, Belorussian, Polish and Slovak populations. However, it is worth noting that Ukrainian sample analyzed in the Rębała et al. study [
      • Rębała K.
      • Mikulich A.I.
      • Tsybovsky I.S.
      • Siváková D.
      • Dzupinková Z.
      • Szczerkowska-Dobosz A.
      • Szczerkowska Z.
      Y-STR variation among Slavs: evidence for the Slavic homeland in the middle Dnieper basin.
      ] was much smaller than our sample and comprised of haplotypes obtained only for 9 Y-STRs. This example emphasizes the need for further studies of Slavic populations, utilizing high-resolution approach, to elucidate subtle differences between those closely related groups.
      All population data described in this paper has been uploaded to the YHRD [

      YHRD 3.0 Y Chromosome Haplotype Reference Database, http://www.yhrd.org/ (Release 39 built at: 10 February 2012).

      ]. This paper follows the guidelines for publication and population data requested by the journal [
      • Carracedo A.
      • Butler J.M.
      • Gusmao L.
      • Parson W.
      • Roewer L.
      • Schneider P.M.
      Publication of population data for forensic purposes.
      ].

      Appendix A. Supplementary data

      The following are Supplementary data to this article:

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