View Full Version : Y chromosomal haplogroup J as a signature of the post-neolithic colonization of Eur.

Monday, August 23rd, 2004, 11:46 PM
Y chromosomal haplogroup J as a signature of the post-neolithic colonization of Europe
F. Di Giacomo1, F. Luca2, L. O. Popa3, N. Akar4, N. Anagnou5, 20, J. Banyko6, R. Brdicka7, G. Barbujani8, F. Papola9, G. Ciavarella10, F. Cucci11, L. Di Stasi12, L. Gavrila3, M. G. Kerimova13, D. Kovatchev14, A. I. Kozlov15, A. Loutradis16, V. Mandarino2, C. Mammi17, E. N. Michalodimitrakis5, 21, G. Paoli18, K. I. Pappa5, 20, G. Pedicini19, L. Terrenato1, S. Tofanelli18, P. Malaspina1 and A. Novelletto2

(1) Department of Biology, University Tor Vergata, Rome, Italy
(2) Department of Cell Biology, University of Calabria, Via P. Bucci, 87030 Rende, Italy
(3) Genetics Department, University of Bucharest, Bucharest, Rumania
(4) Pediatrics Department, Ankara University, Ankara, Turkey
(5) School of Medicine, University of Athens , Athens, Greece
(6) University of P. J. Safarik, Kosice, Slovak Republic
(7) Institute for Haematology and Blood Transfusion, Prague, Czech Republic
(8) Department of Biology, University of Ferrara, Ferrara, Italy
(9) Centro Regionale di Immunoematologia e Tipizzazione Tissutale, LAquila, Italy
(10) IRCCS Casa Sollievo della Sofferenza, S. Giovanni Rotondo, Italy
(11) Az. Osp. Perrino, Brindisi, Italy
(12) A.S.L. 1, Paola, Italy
(13) Department of Hygiene, Azerbaijan Medical University, Baku, Azerbaijan
(14) Department of Biology, Medical University, Varna, Bulgaria
(15) Arct-An C Innovative Laboratory, Moscow, Russian Federation
(16) Ministry of Health Center for Thalassemia, Athens, Greece
(17) A.S.L. BMM, Reggio Calabria, Italy
(18) Department of Ethology, Ecology and Evolution, University of Pisa, Pisa, Italy
(19) Az. Osp. Rummo, Benevento, Italy
(20) Institute of Molecular Biology and Biotechnology, Heraklion, Greece
(21) University of Crete School of Medicine, Laboratory of Toxicology and Forensic Medicine, Heraklion, Crete

Received: 2 February 2004 Accepted: 21 June 2004 Published online: 21 August 2004

Abstract In order to attain a finer reconstruction of the peopling of southern and central-eastern Europe from the Levant, we determined the frequencies of eight lineages internal to the Y chromosomal haplogroup J, defined by biallelic markers, in 22 population samples obtained with a fine-grained sampling scheme. Our results partially resolve a major multifurcation of lineages within the haplogroup. Analyses of molecular variance show that the area covered by haplogroup J dispersal is characterized by a significant degree of molecular radiation for unique event polymorphisms within the haplogroup, with a higher incidence of the most derived sub-haplogroups on the northern Mediterranean coast, from Turkey westward; here, J diversity is not simply a subset of that present in the area in which this haplogroup first originated. Dating estimates, based on simple tandem repeat loci (STR) diversity within each lineage, confirmed the presence of a major population structuring at the time of spread of haplogroup J in Europe and a punctuation in the peopling of this continent in the post-Neolithic, compatible with the expansion of the Greek world. We also present here, for the first time, a novel method for comparative dating of lineages, free of assumptions of STR mutation rates.

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Monday, August 23rd, 2004, 11:49 PM

The extant distribution of Y chromosomal diversity is being increasingly used as a tool for reconstructing the peopling of the world by modern humans, at least from a male perspective (for reviews, see Underhill et al. 2001; Jobling and Tyler-Smith 2003). Major advancements in this field derive from (1) the discovery of numerous single nucleotide polymophisms (SNPs) and other polymorphisms at biallelic loci; (2) the possibility of investigating a further level of diversity determined by multiallelic simple tandem repeat loci (STR). The first set of markers (polymorphisms) has been used to reconstruct a robust phylogeny of the molecular types found today, based on the assumption of a monophyletic origin of the derived allele at each locus, to generate the so-called unique event polymorphism (UEP). The phylogeny is under continuous revision and has been given a unified nomenclature system (Y Chromosome Consortium 2002) to identify each internal UEP-defined lineage or haplogroup. Markers of the second set (STRs) are characterized by mutation rates far higher than in the first set and by a mutational pattern commonly leading to alleles equal in state. By virtue of these properties, STR markers accumulate variation within each haplogroup (de Knijff 2000). When the bulk of STR variation is subdivided according to the different haplogroups, a large part of the homoplasy between allelic states is resolved (Bosch et al. 1999; Forster et al. 2000), allowing us to reconstruct possible evolutionary paths (networks; Bandelt et al. 1999) with a manageable number of reticulations.

STR variation accumulates over time, and a variety of measures and methods have been devised to exploit this process and to infer the antiquity of the corresponding haplogroup (Bandelt et al. 1999; Goldstein et al. 1995; Stumpf and Goldstein 2001; Wilson and Balding 1998). While these methods represent genuine attempts to arrive at absolute dating estimates based solely on genetic data, they rely on a necessary parameter, i.e., the mutation rate at the loci under study, which is in turn the main determinant of the speed of the accumulation process. By virtue of the rare occurrence of each event, the measurement of mutation rate intrinsically suffers from large sampling errors. Large series of father-son transmissions have been examined (Heyer et al. 1997; Foster et al. 1998; Kayser et al. 2000) for a number of STR loci, resulting in estimates that have later been entered into dating studies (e.g. Thomas et al. 1998; Weale et al. 2001; Zerjal et al. 2003). With a few exceptions, the final results in terms of absolute dates are associated with large confidence intervals, and the above considerations prompt us to take them cautiously. A recent attempt to circumvent this problem has been proposed by Zhivotovsky et al. (2004) who have obtained an average mutation rate from population data rather than family data and used known foundation events as starting points for the production of the level of diversity observed today.

Y chromosome diversity across the European continent has revealed high levels of population structuring (Malaspina et al. 2000; Rosser et al. 2000; Semino et al. 2000a). However, different authors attribute the observed patterns of geographic variation to alternative scenarios for the peopling of the continent. In the first, the largest part of diversity is accounted for by a Paleolithic colonization, possibly re-established by Mesolithic repopulation from refugia after the last glacial maximum (LGM; Karafet et al. 1999; Semino et al. 2000a; Underhill et al. 2001; Wilson et al. 2001). In the second, a Neolithic demic diffusion from the Levant was triggered by the development of agricultural practices and introduced into the continent a large proportion of extant types which, despite their appearance, may have predated the migratory movement (Chikhi et al. 2002). Additional observations indicate that further testing of these inferential conclusions is required, e.g., the finding that the distributions of some haplogroups do not fit either model (Jobling and Tyler-Smith 2003), that drift or founder effects may obscure continent-wide distribution patterns (Di Giacomo et al. 2003), and that more recent population expansions and resettlements within the continent could result in spatial patterns resembling those predicted by one or the other of the above-mentioned models.

Testing each of the two models may benefit from the analysis of the appropriate haplogroup(s) in the geographic region(s) that are more informative for its/their dispersal. In this context, time estimates for each lineage are a useful piece of information to reconstruct the tempo of the dispersal and to distinguish between a continuous vs. a punctuated spreading process.

We have addressed the geographic distribution and internal molecular diversity of Y chromosomal haplogroup J in the Middle East, central-eastern Mediterranean, and central-eastern Europe. It is generally agreed that this haplogroup was dispersed by the westward movement of people from the Middle East (Semino et al. 1996, 2000a; Quintana-Murci et al. 2001). Our data show a higher diversity of this haplogroup in areas reached in later phases of this process. Thus, the present-day distribution of haplogroup J cannot be explained by the expansion of a repertoire of types previously present in the area in which this haplogroup supposedly originated.



Our estimates are in agreement with the appearance of J1 and J2 in the Levant at the time of the Neolithic agriculture revolution. Implicitly, this figure makes them of little help in identifying population splitting that may have accompanied the westward dispersal of the entire haplogroup.

Our data and those by Semino et al. (2004) show that J2f1 is predominantly found in the northern Mediterranean, from Turkey westward. In particular, our estimates for this latter sub-haplogroup are barely compatible with its presence among the early Levantine agriculturalists. The coalescence of J2f1 well after the beginning of the Neolithic revolution thus identifies a major population structuring already present at the time of the spreading of haplogroup J in southern Europe and central Mediterranean, thus differentiating the Aegean area from the Middle East. We favor the emergence of J2f1 in the Aegean area, possibly during the population expansion phase also detected by Malaspina et al. (2001) and coincident with the expansion of the Greek world to the European coast of the Black sea. This scenario would agree with the clustering of J2f1 chromosomes in north–west Turkey (Cinnioglu et al. 2004).

We tried to parallel the BATWING analysis with an independent method, free of assumptions concerning STR mutation rates. Indeed, inter-locus heterogeneity for mutation rates is responsible for a large part of variation in dating estimates (Stumpf and Goldstein 2001). This method provides a formal approach to the concept of comparative dating (Malaspina et al. 2001) by exploiting the UEP–STR data set to its fullest extent. Compared with the dating of a single haplogroup or sub-haplogroup, as implemented in YMRCA, it seems more powerful in detecting the signal of increasing diversity with time over the noise of the poor correlation between ASD and time observed for some loci. This is achieved by including, in the analysis, information concerning UEP phylogeny, which provides a unique solution for the order of nodes in the tree to be analysed. As the number of UEP-defined lineages in the Y phylogeny is steadily increasing, this method will become of wider applicability.

Our method has been able to rank the five loci used here in the same order as BATWING according to their mutation rates, indicating that the two programs can detect the same basic trend. In particular, the remarkable evolutionary stability of the marker DYS392 has emerged, in agreement with its constancy in many sets of Y chromosomes typed (Bosch et al. 1999; Forster et al. 2000; Thomas et al. 2000; Nebel et al. 2001; Weale et al. 2001; Cinnioglu et al. 2004). This enables us to review, on a microevolutionary basis, the estimates based on direct observation of father–son transmissions (Heyer et al. 1997; Bianchi et al. 1998; Kayser et al. 2000), a result that may be relevant in forensic applications.

The ASD vs. time method returns relative timings for the branching within the J tree in close agreement with those of BATWING. In particular, it shows a burst of UEP radiation in the second half-life of the entire J haplogroup, followed by the origin of J2f1 in recent times. Unless assuming the origin of J at >50–100 thousand of years ago, this is again incompatible with an J2f1 origin in the Levant at the time of the rise of agriculture.

In summary, our data are in agreement with a major discontinuity for the peopling of southern Europe. Here, haplogroup J constitutes not only the signature of a single wave-of-advance from the Levant but, to a greater extent, also of the expansion of the Greek world, with an accompanying novel quota of genetic variation produced during its demographic growth. In the analysis by Cavalli-Sforza et al. (1994), the two peopling contributions can be distinguished, as they are caught in the first and the fourth principal component, respectively, but the relevance of the latter may have been underestimated. The two processes, widely spaced in time, are associated with dramatically different travel technologies. This implies that, in the central and west Mediterranean, the entry of J chromosomes may have occurred mainly by sea, i.e., in the south–east of both Spain and Italy.

Acknowledgments We gratefully acknowledge Dr. Vincent Macaulay for critically reviewing this manuscript during its preparation. We thank the anonymous reviewers for their useful comments. This work was supported by grant PRIN-MIUR 2002, 2003 to A.N. and PRIN-MIUR 2003 to G.Pa. Sampling in Russia was carried out within the frame of a Science and Technology Cooperation agreement between Italy and Russia (P.M. and A.I.K.: principal investigators).


Wednesday, August 25th, 2004, 06:10 PM
Y chromosomal haplogroup J as a signature of the post-neolithic colonization of Europe

Very useful information. Would you be able to attach a copy of the PDF file?

Wednesday, August 25th, 2004, 06:18 PM
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Sunday, August 29th, 2004, 12:41 AM
Very useful information. Would you be able to attach a copy of the PDF file?

There is no PDF file :(

Monday, August 30th, 2004, 07:16 PM
There is no PDF file :(