Various episodes of population movement have affected southeast Europe, and the role of the Balkans as a long-standing gateway to Europe from the Near East is illustrated by the phylogenetic unification of Hgs I and J by the basal M429 mutation.31
This evidence of common ancestry suggests that ancestral IJ-M429*
Y chromosomes probably entered Europe through the Balkan route sometime before the Last Glacial Maximum. They subsequently evolved into Hg J in the Middle East and Hg I in Europe in a typical disjunctive phylogeographic pattern. Such a geographic corridor is likely to have experienced additional subsequent gene flows, including the migration of agricultural colonists from the Middle East. Pottery is a useful proxy for the spread of farming both spatially and temporally. The first appearance of pottery in the Adriatic region was in Corfu at 6500 BC and reached the northern most Adriatic ~1000 years later.21
Its dispersal provides a comparative template for spatial and temporal patterns of Y chromosome Hg diversity observed in this area.
Hg J is most common (~50%) in the Middle East and Anatolia,27, 29, 47
with a spread zone spanning from northwest Africa to India.12, 55
It has been related to different Middle Eastern migrations.12, 56
In addition to Hg J-M410, Hg G-P15 chromosomes, which are also common in Anatolia,29
have been implicated in the colonization and subsequent expansion of early farmers in Crete, the Aegean and Italy.38, 46, 47, 48
Earlier studies have concluded that the J-M410 sub-clades, J-DYS445-6 and J-M67, are linked to the spread of farming in the Mediterranean Basin,38, 47
with a likely origin in Anatolia.29
Interestingly, J-DYS445-6 and J-M92 (a sub-lineage of M67), both have expansion times between 7000 and 8000 years ago (), consistent with the dating of the arrival of the first farmers to the Balkans. The first detection of milk residue in ceramic pottery occurs in sites from northwest Anatolia 7000–8500 years ago,58
an age that approximates the Hg-expansion times.
Ages of microsatellite variation and mean variance of microsatellite loci within haplogroups
Regarding Hg J-M12/M102, which is discernable from India to Europe, the M12/M102*
chromosomes display a very high YSTR diversity, whereas on the other hand, the J-M241 sub-lineage has low diversity () in the Balkans, indicating different demographic histories. Although Hg J-M241 shows high variance in India,37
its place of origin is still uncertain. As J-M241 has older expansion times in Sicily, Apulia and Turkey (), it may have arrived in the Balkans from elsewhere.
Ages of microsatellite variation and mean variance of microsatellite loci within J-M241 haplogroup in Turkey, the Balkans and Italy
On the other hand, the expansion times of Hg V13 () are consistent with a late Mesolithic time frame. The Greek Mesolithic, although different in its material culture from the Natufian Mesolithic of the Levant, bears some resemblance to the Mesolithic of southern Anatolia.60
This archaeological congruence between the Mesolithic of the Balkans and southern Anatolia may mirror the similar E-V13 expansion times observed for Konya, Franchthi Cave and Macedonian Greece, all approximately 9000 years ago. Moreover, E-V13 YSTR-related data from Bulgaria and Macedonia,28
both with a variances of 0.28, suggest an expansion time of approximately 10
000 years ago. It is likely that the origin of V13 occurred somewhere within the zone of these sample collections. In addition, it is also worth noting that in the Anatolian region of supposed Einkorn wheat origin61
(region 5 of Cinnioglu et al29
), only one V13 chromosome out of 43 is found (PA Underhill, unpublished data). Therefore, as no evidence at present supports the association of E-V13 Hg with the attested origin of farming in southeast Anatolia, the possibility of farming adoption by Balkan E-V13-associated people is plausible. The low E-V13 frequency and STR variation observed in Crete38
indicate that if the first Neolithic colonists came from central Anatolia, they did not bring this Hg. The two more recent expansion times for V13 for Greece and Sesklo and Dimini (), dating to the Bronze Age, possibly reflect a more recent integration of some V13 chromosomes into the populations of the first farmers represented by J-M410 and G-M201 lineages. Both the lack of any plausible Middle Eastern source of E-V13 during either the early Neolithic or Bronze Age and the age of microsatellite variation observed are consistent with E-V13 chromosomes reflecting a Mesolithic heritage as suggested by King et al.38
Ages of microsatellite variation and mean variance of microsatellite loci within E-V13 haplogroup in Turkey and Greece
As reported earlier,28
both J-M12 and E-V13 radiation patterns overlap geographically in the Balkans (). Although J-M12 chromosomes were not genotyped for M241 by Cruciani et al
the low YSTR diversity observed suggests that these are predominantly M241 derivatives. The difference between E-V13 and J-M241 () indicates that both E-V13 frequency and haplotype diversity would have been greater than J-M241 components just before the episode of population growth. This also is the case when the dating is carried out by disregarding the mutational steps connecting the three haplotypes that, including Turkish samples (Supplementary Figure S2), can be considered as founders.62
Whether or not E-V13 and J-M241 participated in the same demography remains uncertain.
The presence of E-M78*
Y chromosomes in the Balkans (two Albanians), previously described virtually only in northeast Africa, upper Nile,28, 63
gives rise to the question of what the original source of the E-M78 may have been. Correlations between human-occupation sites and radiocarbon-dated climatic fluctuations in the eastern Sahara and Nile Valley during the Holocene64
provide a framework for interpreting the main southeast European centric distribution of E-V13. A recent archaeological study reveals that during a desiccation period in North Africa, while the eastern Sahara was depopulated, a refugium existed on the border of present-day Sudan and Egypt, near Lake Nubia, until the onset of a humid phase around 8500 BC (radiocarbon-calibrated date). The rapid arrival of wet conditions during this Early Holocene period provided an impetus for population movement into habitat that was quickly settled afterwards.64
representatives, although rare overall, still occur in Egypt, which is a hub for the distribution of the various geographically localized M78-related sub-clades.28
The northward-moving rainfall belts during this period could have also spurred a rapid migration of Mesolithic foragers northwards in Africa, the Levant and ultimately onwards to Asia Minor and Europe, where they each eventually differentiated into their regionally distinctive branches.
Differently from the earlier discussed Hgs, I-M423 represents the southeast European autochthonous clade of I-P37.2. Its distribution reaches Anatolia, where, however, it is only sporadically observed (2.6%, updated from Rootsi et al23
). Also, virtually, all the I-P37.2*
paragroup members identified in this survey harbouring the peculiar DYS388-15 trinucleotide repeat motif (not observed in any other Hg I clade) likely represent a new rare P37.2 sub-clade. Their distribution (Supplementary Table S1) and the associated YSTR variation age of ~4000 years () suggest that they expanded demographically, perhaps from central European regions during the Bronze Age. In this scenario, the only I-P37.2*
chromosome observed in Albania, not characterized by the unusual DYS388-15 repeat motif marker, could either represent the consequence of a reversion event back to the ancestral allele or be a rare representative of the ancestral P37.2 state.
The network of the STR haplotypes identified in 222 Y chromosomes belonging to the I-M423 Hg (Supplementary Figure S1) is characterized by a star-like shape centred on the most frequent and diffused haplotype that is present in all Balkan populations. The marginal positions occupied by the three Turkish chromosomes are in agreement with a recent gene flow. The age of accumulated microsatellite variation associated with Hg I-M423 () dates to around 8000 years ago (Early Holocene). Thus, although Hgs G and J mark the successful colonization and subsequent demic expansions of Neolithic pioneers to these regions, consistent with a wave of advance,19, 65
the widespread adoption of farming by Mesolithic hunter-gatherers in the Balkans and Central Europe is recorded in the autochthonous Hg I-M423.
These data indicate the complex interactions between farmers and foragers rather than the large-scale replacement of hunter-gatherers by pioneering agriculturalists during the spread from the Neolithic to the southeast Europe. The data also indicate that I-M423 and probably also E-V13 representatives would have been well established in the Balkans before the arrival of a nucleus of pioneering agriculturalists.
Thus, unlike Crete, southern and central Italy and the southern Caucasus, the cultural transmission of the Neolithic package played an important role. Either the initial G and J2 Hg agriculturalists who colonized the Balkans at first flourished but later diminished in a similar manner to that proposed regarding the Linearbandkeramik in central Europe66
or the package was rapidly and robustly adopted by local Mesolithic people in the southern Balkans (plausibly characterized by E-V13), who underwent a demic expansion and a subsequent range expansion to the eastern Adriatic. These former foragers who had recently acquired the Neolithic tradition participated in ‘leapfrog' colonizations up the Adriatic, where they eventually transmitted agricultural practices to resident Mesolithic populations represented by I-M423 chromosomes.
Interestingly, the derived Y-chromosome scenario strongly recalls the fourth PC synthetic map of Europe calculated on gene frequencies at 95 nuclear loci,11
which displays a centre in the southern Balkans and a large surrounding area that terminates with a ‘propagule' to the northeast of the central Balkans. On the basis of this observation, our assumptions could provide a possible interpretation of the described expansion centred in the southern Balkans.