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Keywords:

  • Y chromosome;
  • Y-STRs;
  • radiation;
  • Western Europe;
  • Y-chromosomal subhaplogroups;
  • genetic discrimination

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information

Y-chromosomal short tandem repeats (Y-STRs) are often used in addition to Y-chromosomal single-nucleotide polymorphisms (Y-SNP) to detect subtle patterns in a population genetic structure. There are, however, indications for Y-STR haplotype resemblance across different subhaplogroups within haplogroup R1b1b2 (R-M269) which may lead to erosion in the observation of the population genetic pattern. Hence the question arises whether Y-STR haplotypes are still informative beyond high-resolution Y-SNP genotyping for population genetic studies. To address this question, we genotyped the Y chromosomes of more than 1000 males originating from the West-European regions of Flanders (Belgium), North-Brabant and Limburg (the Netherlands) at the highest resolution of the current Y-SNP tree together with 38 commonly used Y-STRs. We observed high resemblance of Y-STR haplotypes between males belonging to different subhaplogroups of haplogroup R-M269. Several subhaplogroups within R-M269 could not be distinguished from each other based on differences in Y-STR haplotype variation. The most likely hypothesis to explain this similarity of Y-STR haplotypes within the population of R-M269 members is a recent radiation where various subhaplogroups originated within a relatively short time period. We conclude that high-resolution Y-SNP typing rather than Y-STR typing might be more useful to study population genetic patterns in (Western) Europe.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information

The unique biology of the nonrecombining part of the human Y chromosome has led to the widespread use of Y-chromosomal molecular markers in population genetic studies as well as in evolutionary, anthropological, genealogical and forensic research (Jobling & Tyler-Smith, 2003). Population genetic studies use Y-chromosome evolutionary lineages, that is, haplogroups, as discrete categorical variables in order to infer differences among and within the study populations (Jobling et al., 2004). Single-nucleotide polymorphisms (Y-SNP) are most appropriate to define these haplogroups due to their much lower mutation rate compared to short tandem repeat polymorphisms (Y-STRs; Ballantyne et al., 2010). On the other hand, because of their larger allelic range and higher mutation rate (and consequently, higher variance), Y-STRs are also often used in addition to Y-SNPs in population genetic studies as they exhibit a higher degree of variation – and hence, discrimination power – and therefore might allow the detection of more subtle processes in the population (Rebala et al., 2013). However, there are indications that Y-STR haplotype matches based on the widely used 17 Y-STR loci included in the AmpFlSTR Yfiler kit (Applied Biosystems, Foster City, CA, USA) between unrelated individuals exist (Hanson & Ballantyne, 2007) and that the Y-STR haplotype resemblance across different subhaplogroups might lead to erosion in the observation of the population genetic structure in Western Europe, especially within the highly frequent haplogroup R1b1b2 (R-M269; Larmuseau et al., 2012a). Therefore, the question arises whether Y-STR haplotypes within R-M269 are still informative in addition to Y-SNP genotyping for population genetic studies in Western Europe.

To answer this research question, the West-European region of Flanders (Belgium) and the provinces of North Brabant and Limburg (the Netherlands) were selected as the study area since Y-chromosome variation and distribution have already been characterised in detail (Larmuseau et al., 2011, 2012a, b, 2013b). More than 1000 Y chromosomes of males originating from this region were genotyped at the finest known resolution of the latest updated Y-chromosomal tree published by Van Geystelen et al. (2013b), 60% of which fall within haplogroup R-M269. By supplementing this data set with an extensive set of 38 Y-STRs, including the commonly used 17 Y-STRs targeted by the commercial AmpFlSTR Yfiler kit (Butler, 2011), we aimed to investigate the relationship of Y-STR haplotypes with the observed Y-chromosome subhaplogroups to assess the phylogenetic value of Y-STRs within haplogroup R-M269. This was done (1) by comparing subhaplogroup memberships of similar Y-STR haplotypes within haplogroup R-M269, (2) by comparing R-M269-associated Y-STR haplotypes between subhaplogroups in a network analysis and (3) by comparing the consensus haplotypes for each of the subhaplogroups based on the modal alleles per Y-STR locus.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information

Sampling Procedure

Samples were selected from the ongoing open genealogical project “DNA Brabant/Belgium” that includes participants whose oldest reported patrilineal ancestor (ORPA) lived in Flanders (Belgium), North Brabant or Limburg (The Netherlands) before the year 1800. All samples have been collected with written consent from the donors who gave permission for the DNA analyses, storage of the samples and scientific publication of their anonymised DNA results.

DNA Extraction and Genotyping

A buccal swab sample from each selected participant was collected for DNA extraction by using the Maxwell 16 System (Promega Corporation, Madison, WI, USA) followed by real-time PCR quantification (Quantifiler Human DNA kit, Applied Biosystems). In total, 38 Y-STR loci were genotyped for all samples as described previously (Larmuseau et al., 2012b). The whole process was reproduced with new primer sets for all individuals that showed nonamplified loci, in order to exclude failure due to technical errors or mutations in the standard primer positions.

All haplotypes were submitted to Whit Athey's Haplogroup Predictor (Athey, 2006) to obtain probabilities for (broad) haplogroup membership. Based on these results, the samples were assigned to specific Y-SNP genotyping assays to confirm the predicted broad haplogroup and to assign the subhaplogroup to the most detailed level of the latest published Y-chromosomal tree (Van Geystelen et al., 2013b). The recently characterised Y-SNPs that improved resolution of R-M269 phylogeny were included (Fig. 1). Seventeen multiplex systems, targeting a total of 120 Y-SNPs, were developed using SNaPshot mini-sequencing assays (Applied Biosystems) according to previously published protocols (Caratti et al., 2009; Van Oven et al., 2011b). A fraction of the participants were already partly genotyped in previous studies (Larmuseau et al., 2012a, b).

image

Figure 1. Phylogenetic relationships of all analysed binary markers within the Y-chromosome haplogroup R-M269. The nomenclature of the subhaplogroups is based on the terminal mutation that defines them. Commonly used synonyms of certain Y-SNPs are mentioned as well.

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Statistical Analysis

GenAlEx version 6.5 (Peakall & Smouse, 2006, 2012) was used to find the sample pairs matching at (1) the commonly used 17 Y-STR loci of AmpFlSTR Yfiler and at (2) the full set of 38 genotyped Y-STR loci, respectively. Subhaplogroup affiliation, as well as the in-depth genealogy of the donors of sample pairs with similar haplotypes, were compared with each other. The mutational processes generating null alleles, insertions and microvariants are expected to occur at a lower rate than the stepwise mutations characteristic for Y-STRs (Balaresque et al., 2009; Myres et al., 2009). Therefore, it is possible that they are phylogenetically more robust and can better differentiate subhaplogroups than Y-STRs do according to the single stepwise mutation model. All null alleles, insertions and microvariant alleles were checked for their ability to differentiate subhaplogroups within R-M269.

Median-joining haplotype networks for each of the observed subhaplogroups within the R-M269 radiation were constructed based on all 26 genotyped single-copy Y-STRs (multicopy Y-STRs are not suitable for network construction) by NETWORK version 4.5.1.0 (Bandelt et al., 1999; http://www.fluxus-engineering.com) using the weighting scheme described by Qamar et al. (2002) which is in agreement with the locus-specific mutation rates reported by Ballantyne et al. (2010). For each subhaplogroup within R-M269, six random samples of unrelated persons were used to construct the network. We selected only six samples of each subhaplogroup to avoid an incomprehensible tangle. To reduce network complexity, we additionally constructed median-joining haplotype networks based on the 10 Y-STRs (DYS390, DYS392, DYS438, DYS454, DYS455, DYS388, DYS426, DYS448, DYS437 and DYS393) with the lowest mutation rate, maintaining the same weighting scheme described by Qamar et al. (2002).

Finally, the most frequent (modal) alleles, the averages and the variances for the 26 single-copy Y-STRs were estimated for each observed subhaplogroup within the R-M269 radiation. When there was more than one DNA donor per family, only one donor was selected to avoid a family bias. The consensus Y-STR haplotypes for each subhaplogroup consist of the modal allele values at each of the 26 single-copy Y-STRs (Toscanini et al., 2008; Hammer et al., 2009). When two different alleles of a particular Y-STR locus were equally common within one subhaplogroup, both alleles were included in the consensus haplotype for that subhaplogroup. The haplotype variances for each subhaplogroup were calculated using the Vp formula provided in Kayser et al. (2001).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information

Overall, we analysed the Y-chromosomes of 1028 individuals for whom genealogical records, going back to before the year 1800, were collected with considerable efforts to assure high data quality. All Y-STR and Y-SNP data generated in this study have been submitted to the open-access Y-STR Haplotype Reference Database (YHRD, http://www.yhrd.org): accession numbers YA003651-YA003652-YA003653-YA003738-YA003739-YA003740-YA003741-YA003742. All individuals except one were correctly assigned to a broad haplogroup by Whit Athey's Haplogroup Predictor. The single exception was assigned to haplogroup E, but turned out, after Y-SNP genotyping, to belong to haplogroup A, a haplogroup that is not included in Athey's predictor tool. However, according to a recent study on the root of the human Y-chromosomal phylogenetic tree by Scozzari et al. (2012), haplogroup A is not monophyletic and therefore this Y-chromosome is further referred to as belonging to paragroup Y*(xBCDEF). In total, 53 different subhaplogroups were observed in the data set. The subhaplogroup counts and relative frequencies for the full data set based on Y-SNP genotyping are given in Table 1. Sixty-one percent of the individuals fell within the R-M269 radiation. Fourteen different subhaplogroups within R-M269 were observed. Based on the strong differentiation in haplotypes found in the two most basal and low-frequency subhaplogroups (in fact: paragroups) within R-M269, namely R-M269* (19 individuals) and R-P310* (eight individuals), neither lineage is assumed to be part of the R-M269 radiation of Western Europe. Nevertheless, because of the common practice to refer to the observed radiation in R1b1b2 subhaplogroups in Western Europe as the “R-M269 radiation” (Busby et al., 2012), we will still use this term throughout this paper. Five R-M269 subhaplogroups with a frequency exceeding 5% were observed in the population sample: R1b1b2a1a1b2 (R-L48) with 11.8%, R1b1b2a1a2* (R-P312*) with 9.9%, R1b1b2a1a1b* (R-Z381*) with 9.3%, R1b1b2a1a2e* (R-M529*) with 8.1% and R1b1b2a1a2g3 (R-L2) with 5.3%.

Table 1. Distribution and frequency of all observed Y-chromosome subhaplogroups within the Belgian population (including the province of North Brabant in the Netherlands) based on Y-SNP 5 genotyping. The subhaplogroups with a frequency ≥5% are given in bold
(Sub)haplogroupNumberFrequency
Y*(xBT)10.1
E1b1b1* (E-M35.1*)20.2
E1b1b1a1* (E-M78*)10.1
E1b1b1a1a* (E-V12*)10.1
E1b1b1a1b* (E-V13*)282.7
E1b1b1a1c* (E-V22*)40.4
E1b1b1b1* (E-M81*)30.3
E1b1b1c* (E-M123*)20.2
E1b1b1c1* (E-M34*)111.1
G2a* (G-P15*)40.4
G2a3* (G-U8*)302.9
G2a3a1 (G-Page19)10.1
G2a3b1a1* (G-U13*)30.3
I1* (I-M253*)12111.8
I1c (I-P109)70.7
I2* (I-P215*)131.3
I2a* (I-P37.2*)151.5
I2b1* (I-M223*)383.7
I2b1a (I-M284)20.2
I2b1c (I-P78)20.2
I2b1d (I-P95)30.3
J1* (J-M267*)30.3
J1e* (J-P58*)70.7
J2a* (J-M410*)252.4
J2a2* (J-M67*)50.5
J2a2a* (J-M92*)50.5
J2a8 (J-M319)20.2
J2b2* (J-M241*)70.7
L1* (L-M27*)30.3
L2* (L-M317*)10.1
Q1* (Q-P36.2*)30.3
R1* (R-M173*)10.1
R1a1* (R-SRY10831.2*)10.1
R1a1a* (R-M198*)383.7
R1b1* (R-P25*)10.1
R1b1b* (R-P297*)10.1
R1b1b2* (R-M269*)191.8
R1b1b2a1a* (R-P310*)80.8
R1b1b2a1a1* (R-U106*)171.7
R1b1b2a1a1a (R-Z18)201.9
R1b1b2a1a1b* (R-Z381*)969.3
R1b1b2a1a1b2 (R-L48)12111.8
R1b1b2a1a1b1 (R-U198)131.3
R1b1b2a1a2* (R-P312*)1029.9
R1b1b2a1a2d (R-SRY2627)101.0
R1b1b2a1a2e (R-M529)838.1
R1b1b2a1a2g* (R-U152*)333.2
R1b1b2a1a2g3 (R-L2)545.3
R1b1b2a1a2g4 (R-L20)141.4
R1b1b2a1a2h (R-Z195)363.5
T1a2 (T-P77)10.1
T1a4* (T-P321*)10.1
T1b* (T-L131*)50.5
Total1028100.0

Next, sample pairs matching at all 17 Y-STRs of the AmpFlSTR Yfiler, and at the full set of 38 genotyped Y-STRs, respectively, were determined. Although the mutation rate of processes generating null alleles, insertions and microvariants can be assumed to be lower than that of stepwise mutations in Y-STRs, we did not find any null allele, insertion or microvariant allele that was shared by more than one individual per subhaplogroup within R-M269. Null alleles, insertions and microvariants were each considered as single mutation steps, when calculating the matches between individuals. This is a reasonable approach when comparing haplotypes within R-M269 as demonstrated by the following example: two individuals with a most recent patrilineal common ancestor (MRCA) born in 1852 belonged to the same Y-SNP subhaplogroup and shared the same 38-locus Y-STR haplotype except that one individual showed a confirmed nonamplification for Y-STR locus DYS442, most likely due to a mutation in the primer-complementary sequence preventing amplification of the locus.

At the resolution of the 17 Yfiler Y-STRs we identified 98 pairs with identical haplotypes, of which 67 pairs fell within haplogroup R-M269 (Fig. 2). From these 67 pairs, there are 21 pairs of which the members belong to different subhaplogroups of R-M269. Out of the other 46 pairs in which the members do belong to the same subhaplogroup, only 21 pairs have a common patrilineal ancestor within recent centuries based on their documented genealogy. Within all 31 pairs not belonging to haplogroup R-M269, the individuals always belonged to the same subhaplogroup at the finest phylogenetic level. The in-depth genealogical data of 22 pairs of the 31 pairs outside R-M269 also revealed a common documented patrilineal ancestor within the last centuries.

image

Figure 2. Comparison of the subhaplogroups within sample pairs of a perfect match or of a match with one difference based on the 17 Y-STR (Yfiler) haplotype. For pairs in which the samples have the same subhaplogroup a distinction is made between pairs with a legal patrilineal relationship based on their in-depth genealogical records (before 1800) and pairs without such a legal patrilineal relationship. The pairs are classified under “Within R-M269” when the individuals were both assigned to subhaplogroups within R-M269 except of R-M269* and R-P310* haplotypes (upper graph) or under “Other” when the individuals were both assigned to subhaplogroups excluding those within R-M269 (lower graph).

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Next, we found a total of 519 pairs with a 17-Y-STR-match with a single-mutation-step difference, of which 452 pairs were within R-M269. From these 452 pairs there are 314 pairs in which the members belong to different subhaplogroups of R-M269. Of the 67 one-mutation-difference pairs belonging to haplogroups other than R-M269, there was only one pair in which the members belonged to different subhaplogroups, namely I2b* (I-M223*) and I2b4 (I-P95).

There was no pair of either identical (zero differences) or near-identical (one mutation-step difference) Y-STR haplotypes and a known documented common patrilineal ancestor whereby the individuals were assigned to different subhaplogroups, which would have indicated an error either in the genealogy or in the genotyping.

When analysing the Y-STR haplotypes at the resolution of all 38 genotyped Y-STRs, all 26 pairs within R-M269 either with a perfect match, one mismatch or even two mismatches, also belonged to the same subhaplogroup and 16 pairs of them indeed had a documented common recent patrilineal ancestor (Fig. 3). More than 42% of the pairs with three or more differences within R-M269 had a different subhaplogroup assignment. Within other haplogroups, individuals from only two out of 110 pairs belong to a different subhaplogroup with, for both pairs, one individual belonging to I2b* (I-M223*) and the other to I2b4 (I-P95). There was no pair with ≤6 Y-STR differences and with a known documented paternal ancestor where the individuals were assigned to different subhaplogroups.

image

Figure 3. Comparison of the subhaplogroups within sample pairs of a perfect match or of a match with ≤6 differences based on the 38 Y-STR haplotype. For pairs in which the samples have the same subhaplogroup, a distinction is made between pairs with a legal patrilineal relationship based on their in-depth genealogical records (before 1800) and pairs without such a legal patrilineal relationship. The pairs are classified under “Within R-M269” when the individuals were both assigned to subhaplogroups within R-M269 except of R-M269* and R-P310* haplotypes (upper graph) or under “Other” when the individuals were both assigned to subhaplogroups excluding those within R-M269 (lower graph).

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The median-joining haplotype network for R-M269 based on 26 single-copy Y-STR loci revealed that it was not possible to identify clusters in the network that corresponded to the Y-SNP-based subhaplogroups (Fig. 4), except for the six individuals belonging to subhaplogroup R-U198 which were all located on the same branch. The network based on only the 10 lowest mutating Y-STRs does not reveal any clustering either, but only shows high cross-haplogroup resemblance (Fig. S1).

image

Figure 4. Median-joining haplotype network of 72 samples belonging to haplogroup R-M269 (excluding R-M269* and R-P310*) based on 26 single-copy Y-STR loci. Only six haplotypes of unrelated persons were arbitrarily selected for each of the 12 observed subhaplogroups in the population. The colour of the circles represents the subhaplogroup to which the haplotype belongs based on Y-SNP typing.

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Finally, the modal allele, the average and the variance for each of the 26 single-copy Y-STR loci were calculated for each of the observed subhaplogroups of R-M269 (Table S1). All 12 subhaplogroups have an (almost) identical consensus haplotype. The modal allele of one subhaplogroup never varied more than one repeat from the modal alleles of the other subhaplogroups, except for DYS635 within R-U198. Although the modal allele is highly dependent on the sample size for each subhaplogroup, the average allele size together with the modal allele could be compared for each Y-STR locus in all subhaplogroups. Among the 26 Y-STR loci there were only eight loci with one- or two-step differences between consensus haplotypes of the subhaplogroups. Most of these eight Y-STRs have a high mutation rate according to Ballantyne et al. (2010), although also the Y-STR locus with the lowest mutation rate of the genotyped Y-STR set differs in the consensus haplotype of haplogroup R-Z195* (Table S2). Most differences were found for the consensus haplotype of R-U198, with four differences in comparison with the averaged one of the other subhaplogroups within R-M269. The fact that the consensus haplotype for R-U198 was most different from the averaged one for R-M269 is consistent with the observed separate clustering of R-U198 haplotypes in the phylogenetic network (Fig. 4). Two differences were found for the consensus haplotype of R-L20 and one for the consensus haplotypes of R-Z18 and R-L48 in comparison with the averaged one of the other subhaplogroups. No single individual in the data set carried exactly the modal Y-STR haplotype of haplogroup R-M269 or of its specific subhaplogroup. No pattern was seen in the respective Y-STR allelic variances of the subhaplogroups.

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information

By combining Y-SNPs at the currently highest possible phylogenetic level, a set of 38 Y-STRs and extended genealogical data of all DNA donors, this study reveals a strong Y-STR haplotype resemblance among West-European males belonging to haplogroup R-M269, which is most likely the result of rapid population expansion. This expansion event should have been accompanied by an accumulation of allelic variance, such that the action of mutation and genetic drift had no chance to generate distinctive, subhaplogroup-specific haplotypes. As such it is not possible to predict the subhaplogroup within R-M269 to which an individual belongs based on his Y-STR haplotype, in contrast to the situation with higher level haplogroups for which haplotypes do have predictive power (Athey, 2005; Schlecht et al., 2008). The high resemblance of haplotypes across different subhaplogroups of R-M269 is observed (i) based on the comparison of the phylogenetic lineage (subhaplogroup) between similar haplotypes which should reveal a recent genealogical relationship between DNA donors, (ii) based on comparing haplotypes between subhaplogroups in a network analysis and (iii) by exploring the consensus haplotypes for each subhaplogroup based on the modal alleles for all genotyped Y-STRs.

Resemblance of Haplotypes Belonging to Different R-M269 Subhaplogroups

Despite the common use of the commercial AmpFlSTR Yfiler kit in population genetic studies (Butler, 2011), many 17-locus Y-STR matches in our data set are cross-subhaplogroup. Of the R-M269 pairs with a perfect 17-Y-STR match, 31% included members that each belonged to a different subhaplogroup, and among the pairs with a single mismatch this was even as high as 69% (Fig. 2). When the haplotypes were extended to 38 Y-STRs, the subhaplogroups of only the individuals within pairs with less than three mismatches were identical (Fig. 3). Next, individuals of 17-Y-STR and 38-Y-STR match pairs within R-M269 which also belonged to the same subhaplogroup did not always reveal any known documented patrilineal relationship and/or do not have the same (or similar) surname, although this should be the case based on their similarity (Walsh, 2001). Based on extended genealogies, we do not find a genealogical connection between individuals for 55% of the perfect 17-Y-STR matches and 93% of the 17-Y-STR matches with one difference, although the subhaplogroup is identical within those matches (Fig. 2). We also did not find a connection between individuals of 38% of the 38-Y-STR matches with maximally two differences, and of 83% of the 38-Y-STR matches with three to six differences (Fig. 3). In these cases, an (almost) Y-STR-match will most likely be meaningless, although not knowing of patrilineal relatedness could also be the result of unknown/hidden cuckoldry together with nonpaternal surname transmission although the frequency of such events is expected to be quite low (King & Jobling, 2009a, b). Another possibility is that the members of these pairs have a time to most recent common ancestor (tMRCA) that precedes the origin of hereditary surnames, namely the 13th or 14th century (Larmuseau et al., 2013a). Nevertheless, this possibility is also quite unlikely according to the formulae of Walsh (2001) and the Y-STR mutation rates.

The strong resemblance between haplotypes across different subhaplogroups of R-M269 is further illustrated by the median-joining haplotype network based on all 26 genotyped single-copy Y-STRs. This network shows that the haplotypes do not cluster according to their known Y-SNP-based subhaplogroup memberships within R-M269 (Fig. 4). The network based on only the 10 genotyped Y-STRs with the lowest mutation rate did not show any substructure either but rather, only high cross-haplogroup resemblance (Fig. S1). However, networks based on only slower mutating Y-STRs may, in some cases, reveal a stronger phylogenetic signal by reducing the number of reticulations, and thus complexity, of the network (Van Oven et al., 2011a). Moreover, the consensus haplotypes were (nearly) identical among the subhaplogroups within R-M269 (Table S1). The only exception are the haplotypes of subhaplogroup R-U198 which are more closely related to each other than they were to the haplotypes from other R-M269 subhaplogroups (Fig. 4). Nevertheless, these results reveal that the Y-STR haplotypes of most R-M269 subhaplogroups do not reflect the phylogenetic signals within R-M269, not even when using 26 single-copy Y-STRs. Although the samples used in this study are from one specific region in Western Europe, namely Flanders, several phylogenetic groups are independently distributed in Europe and evolved from each other (Busby et al., 2012). Therefore, it is most likely that there is also no geographical differentiation expected within R-M269 based on Y-STRs (at least not at the currently tested resolution level) in contrast to Y-SNP-based subhaplogroups (R-U106, R-P312, R-U152) which show remarkably different localised concentrations at a European scale (Myres et al., 2011; Cruciani et al., 2011). These results illustrate that Y-STR haplotypes, at the resolution of a limited number of Y-STR loci, are not necessarily suitable to infer differences between relatively recently diverged Y-SNP haplogroups, as we here demonstrated for R-M269 subhaplogroups in a West-European population.

Haplotype Resemblance as Result of Recent Radiation(s)

The most likely hypothesis for the high resemblance of haplotypes belonging to several subhaplogroups within R-M269 is a huge recent radiation where the many currently existing R-M269 lineages originated within a relatively short time frame during a fast growth of the population. The time since the subhaplogroups diverged from each other was too short, and the action of random drift too weak, for the respective Y-STR haplotypes to acquire distinctive, subhaplogroup-associated variants. The resemblance of haplotypes from different subhaplogroups within R-M269 is thus most likely the result of identity-by-descent (IBD). Nevertheless, this might be in combination with identity-by-state (IBS) as no single individual carries the modal 38 Y-STR haplotype of haplogroup R-M269 or any of its specific subhaplogroups due to the high Y-STR mutation rate (de Knijff, 2000). The Y-chromosomal haplogroup R-M269 is carried by approximately 110 million European men, increasing in frequency from the east (12% in Eastern Turkey) to the west (85% in Ireland; Myres et al., 2011). The geographic distribution of R-M269 is regarded as the result of a surfing effect, whereby the mutant arose in the wave of a geographically fast expanding population, having an advantage over mutants arising behind the expansion front not due to natural selection but due to random genetic drift (Klopfstein et al., 2006; Chiaroni et al., 2009; Slatkin & Excoffier, 2012; Swaegers et al., 2013). Consistent with our Y-STR haplotype observations, recent next-generation sequencing (NGS) data reveal a huge polytomy and ramification pattern in the phylogenetic tree of R-M269, suggesting indeed the rapid birth of numerous subhaplogroups (Rocca et al., 2012; Francalacci et al., 2013; Wei et al., 2013). Nevertheless, the rapid development of subhaplogroups within R-M269 might be the result of only one main expansion event or of a combination of several (local) expansion processes.

The period during which the fast expansion(s) of the R-M269 male population occurred has been debated for a long time. Previous data on haplogroup R-M269 and statistical modelling have ascribed the cline of R-M269 either to an ancient Paleolithic expansion event (Rosser et al., 2000; Semino et al., 2000; Morelli et al., 2010), or to a more recent Neolithic demic expansion from the Near East through Anatolia (Sjödin & François, 2011, Balaresque et al., 2010). According to the calibrated human Y chromosome phylogeny based on whole genome resequencing data (Wei et al., 2013) and to a wide European phylogeographic analysis based on high phylogenetic resolution within R-M269 (Myres et al., 2011), a postglacial expansion is favoured above a Paleolithic expansion. As more and more resequencing data will become available, future calibration exercises of the Y-chromosome phylogenetic tree will provide more information when this expansion has occurred (Poznik et al., 2013). Although the transition to agriculture was a pivotal event in the Holocene, the spread of several subhaplogroups of R-M269 could have occurred through multiple migration events suggesting more complex postglacial scenarios (Myres et al., 2011; Busby et al., 2012). Since the Holocene, the census population size in Europe has increased dramatically and apparently without intermediate genetic bottleneck events (Busby et al., 2012; Pinhasi et al., 2012), which could explain the lack in Y-chromosome haplotype differentiation between subhaplogroups within R-M269.

It is expected that the final achievable resolution level of the R-M269 phylogeny will be much higher than that of the one currently constructed (Rocca et al., 2012; Francalacci et al., 2013). Nevertheless, the conclusions based on the observed resemblance in Y-STR haplotypes in our study will still be relevant and even better detectable after further optimizing of the Y-chromosome phylogeny. Therefore, future research on the Y-chromosome phylogeny based on whole genome sequencing (WGS) samples as done in Van Geystelen et al. (2013a, b) is useful for population genetics as well as for all other Y-chromosome applications such as forensic sciences and genetic genealogy.

Consequences for Forensic and Genealogic Research

Besides population genetic studies, the present observations also have clear consequences for forensic research and genetic genealogy. Up to now, studies with allele frequencies on the 17 Yfiler loci in specific populations have been published as basic information to perform forensic research using Y-chromosomal molecular markers (Bai et al., 2013; Lowery et al., 2013; Mielnik-Sikorska et al., 2013). Although such studies are useful to obtain reliable population frequencies of the respective haplotypes, for forensic cases it will be important to use more discriminative Y-STRs, which have the ability to differentiate families, family members and even individual males, than the currently commonly used AmpFlSTR Yfiler based on the results of this study. Rapidly mutating Y-STRs (rmSTRs) already proved empirically their suitability for distinguishing closely as well as distantly related males (Hanson & Ballantyne, 2007; Ballantyne et al., 2010, 2012). rmSTRs, however, will have a mutation rate too high to estimate the surname or designate the family of an unknown male, as was already suggested for the British population based on a limited number of Y-STRs (King et al., 2006; King & Jobling, 2009b). For many 17-Y-STR matches no patrilineal relationship or shared surname is guaranteed between a DNA donor in a database and the DNA sample from a crime scene (King & Jobling, 2009b). For such applications it will be useful to use more than the 17 commonly used Y-STRs, or to supplement the Y-STRs with a suitable panel of Y-SNPs offering (very) detailed phylogenetic resolution. The recently developed PowerPlex Y23 multiplex kit (Promega Corporation) which is an enlargement of AmpFlSTR Yfiler with six extra Y-STRs will show fewer matches between unrelated males (Coble et al., 2013; Davis et al., 2013; Thompson et al., 2013). Finally, to estimate the geographic origin of an unknown person it is important to take also Y-SNPs into account rather than just Y-STRs because of the high Y-STR haplotype resemblance across different subhaplogroups within R-M269. At the finest phylogenetic resolution there are many differences in the frequency of the subhaplogroups on a continental scale (Cruciani et al., 2011; Myres et al., 2011) and even on a small geographical scale (Brion et al., 2004; Larmuseau et al., 2011, 2012b). This makes the use of Y-SNPs, rather than Y-STRs, more relevant in forensic cases to locate the most likely geographic origin of an unknown male based on his Y-chromosome. In recent decades, the use of Y-STRs in the latter forensic application, inference of geographic origin, has been driven by their relative lack of ascertainment bias compared to Y-SNPs. With the higher resolution of the current Y-chromosomal phylogeny due to NGS, the ascertainment bias of Y-SNPs is falling. Hence, the advantages of Y-STRs will decrease in comparison with Y-SNPs to locate the most likely geographic origin of a DNA donor.

The high chance of false positive Y-STR matches within R-M269 also has consequences in genetic genealogy, especially to find unknown patrilineal relatives. In this study, for example, two individuals with a patrilineal genealogical origin in the same Flemish region had a 38-locus Y-STR haplotype near-match with different alleles at three loci. Based on the formulae of Walsh (2001) to estimate the time of the most recent ancestor (tMRCA) their MRCA should have lived between 4 and 35 generations ago (95% confidence interval), hence maximally 875 years ago assuming a generation time of 25 years. Nevertheless, the two individuals turned out to belong to different subhaplogroups within R-M269 so the tMRCA of the males must be between 4.3 and 13 thousand years ago as estimated by Wei et al. (2013), a timescale that is totally useless for genealogical purposes. The results of our study showed no cross-haplogroup resemblance of 38-locus Y-STR haplotype matches with less than three mutational differences, suggesting that comparing haplotypes based on a larger number of Y-STR loci may more reliably reveal true patrilineal relatedness, as expected. Therefore, a large panel of Y-STRs and/or Y-SNPs is crucial to find and verify presumed genealogical connections both for amateur genealogists and for academic researchers using genetic genealogy (Larmuseau et al., 2013a). Finally, the results are also relevant in the light of a recent publication by Gymrek et al. (2013) demonstrating the possibility to identify personal genomes by Y-STR matches, surname inference and public databases. The resemblance in Y-chromosomal haplotypes observed in our study indicates that only in specific cases will the method described by Gymrek et al. (2013) be successful in revealing the identity of an anonymised genome.

Acknowledgement

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information

We thank all the volunteers who donated DNA samples. We acknowledge the Flemish society for genealogical research “Familiekunde Vlaanderen,” as well as Marc Van Den Cloot and Marc Gabriëls, who were involved in the collection of the samples. We thank two anonymous reviewers for improving a previous version of this manuscript, Luc De Meester, Jean-Jacques Cassiman, Lucie Larno, Marie Boz, Hendrik Larmuseau and Lucrece Lernout for useful assistance and discussions. MHDL is postdoctoral fellow of the FWO-Vlaanderen (Research Foundation-Flanders). MvO was supported in part by a grant from the Netherlands Genomic Initiative (NGI)/Netherlands Organization for Scientific Research (NWO) within the framework of the Forensic Genomics Consortium Netherlands (FGCN). This study was funded by the Flemish Society for Genealogical Research “Familiekunde Vlaanderen” (Antwerp), FWO-Vlaanderen, the Flanders Ministry of Culture and the KU Leuven BOF-Centre of Excellence Financing on “Eco- and socio-evolutionary dynamics” (Project number PF/2010/07).

Ethical Standards

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information

The authors declare that the experiments fully comply with the current laws of the country in which they were performed, namely Belgium.

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  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information
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Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. Ethical Standards
  9. Conflict of Interest
  10. References
  11. Supporting Information

Disclaimer: Supplementary materials have been peer-reviewed but not copyedited.

FilenameFormatSizeDescription
ahg12050-sup-0001-TableS1.docx204K

Table S1 Modal allele, average and variance of all 26 single-copy Y-STRs for all R-M269 individuals (excluding R-M269* and R-P310*) and for all the other 12 subhaplogroups within R-M269 separately.

Table S2 Mutation rate of all genotyped Y-STRs based on Ballantyne et al. (2010) and Chandler (2006).

Figure S1 Median joining network of the 10-Y-STR haplotypes belonging to all subhaplogroups within haplogroup R-M269 observed in the data set except for R-M269* and R-P310* haplotypes.

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