Clinal patterns of human Y chromosomal diversity in continental Italy and Greece are dominated by drift and founder effects

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Abstract

We explored the spatial distribution of human Y chromosomal diversity on a microgeographic scale, by typing 30 population samples from closely spaced locations in Italy and Greece for 9 haplogroups and their internal microsatellite variation. We confirm a significant difference in the composition of the Y chromosomal gene pools of the two countries. However, within each country, heterogeneity is not organized along the lines of clinal variation deduced from studies on larger spatial scales. Microsatellite data indicate that local increases of haplogroup frequencies can be often explained by a limited number of founders. We conclude that local founder or drift effects are the main determinants in shaping the microgeographic Y chromosomal diversity.

Introduction

The non-recombining portion of the human Y chromosome (NRY) is widely used as a marker of inter-population divergence. Since the NRY does not undergo recombination, it formally behaves as a single locus with many alleles. These are called haplotypes or haplogroups (Hg) depending on the type of variation used to define them.

For single nucleotide polymorphism (SNP) variation, the phylogenetic relationships among Hg’s can be reconstructed unequivocally, assuming a monophyletic origin of the derived state at each variant position. Experimental data have not contradicted this assumption and a comprehensive tree has been recently presented (YCC, 2002). A notable feature of this tree is the presence of 18 major clades defined by a limited number of mutations. Chromosomes belonging to some clades are confined to specific continents. Thus, geographic distribution of Hg’s can be used as a powerful tool to shed light on population affinities and male-mediated gene flow and admixture.

An additional type of variation which has been used to address these questions is represented by microsatellite markers (STR), which can be arrayed into haplotypes. The most promising approach combines the analysis of these two types of polymorphisms to describe the variation of fast-evolving STRs within each SNP-defined lineage (de Knijff, 2000). STR allele size distributions in fact convey information on each lineage antiquity and the population demography underlying its dispersal (King et al., 2000 and references therein).

Several studies have shown that the NRY markers display the highest quotas of inter-population divergence ever reported for human populations (Hammer and Zegura, 2002; Romualdi et al., 2002). The causes of this are currently debated, and may not be necessarily the same when considering different geographic scales (i.e., continental vs. local; Hammer et al., 2001). In a survey of European data spanning over 1000 km, NRY markers displayed a higher rate of spatial divergence among populations than the one observed for mitochondrial and autosomal markers (Seielstad et al., 1998). These authors attribute their observation to a higher female migration rate. These findings suggest that NRY diversity may be used to reveal population structuring also on a micro-geographical scale, allowing the analysis of genetic consequences of peopling events, population spread, gene flow, and admixture for local areas (Lell and Wallace, 2001; Renfrew, 2001).

Previous studies have showed that, using a limited number of NRY markers and the appropriate sampling scheme, it is generally possible to recognize distinct geographical patterns across Europe (Malaspina et al., 1998, Malaspina et al., 2000; Rosser et al., 2000; Semino et al., 2000; Stefan et al., 2001).

In this paper we describe micro-geographic variation of nine NRY Hg’s from thirty male groups sampled in Italy and Greece. The aim of this study is to test alternative expectations on micro-geographic Hg distributions, i.e., clinal distributions reflecting those reported throughout Europe, abrupt changes in Hg frequencies reflecting sharp genetic boundaries, absence of relevant geographic patterning.

Section snippets

The subjects

We analyzed blood samples from a total of 890 male subjects with known parental and granparental origins: 524 Italians (locations 1–17 in Table 1 and Fig. 1), 154 individuals from continental Greece (locations 18–24), 212 subjects from Crete (locations 25–28), and the Aegean islands of Lesvos and Chios (locations 29–30).

Informed consent was obtained in all cases. Sampling was anonymous in order to prevent link to the original donor.

The markers

We used the SNPs at DYS257, SRY10831, DYS221136, M170, and

Hg frequency distribution in Italy and Greece

Within each country we found a highly significant heterogeneity of Hg frequencies (Table 1; χ2=210, 128 d.f., p=.0001 for Italy and χ2=134, 96 d.f., p=.005 for Greece).

The 9 NRY markers allow the identification of Hg’s in the vast majority of subjects, since only 6.3% (Italy) and 7.7% (Greece) of the chromosomes were unassigned. Interestingly, in Greece more than one fourth of these chromosomes are found in a single location from Crete. Only a single Hg A individual was found, a finding which

Conclusions

Previous studies describing clinal variation of Y chromosome diversity were generally based on samples supposedly representative of entire national communities or ethnic groups. Even in cases where representativeness of the sample is taken into account, this method implicitly reduces the complexity of spatial variation since the “clinal” description of the variation is largely the result of interpolation. This effect is further enhanced when the description of trends is pursued with smoothing

Acknowledgements

We thank Prof. G. Barbujani for the VAL samples and for helpful comments on a first draft of this paper. We are grateful to Dr. M. Hammer for providing details of the DYS221136 assay and to Dr. M. Jobling for control samples. The comments of three anonymous reviewers are gratefully acknowledged. Work supported by grants Agenzia 2000 and PRIN 2002 to A.N. and P.M. and CNR Grant 01.00646.PF36 to L.T.

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