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Title: A Predominantly Neolithic Origin for European Paternal Lineages}
Article:
Abstract:
The relative contributions to modern European populations of Paleolithic hunter-gatherers and Neolithic farmers from the Near East have been intensely debated. Haplogroup R1b1b2( R-M269) is the commonest European Y-chromosomal lineage, increasing in frequency from east to west, and carried by 110 million European men. Previous studies suggested a Paleolithic origin, but here we show that the geographical distribution of its microsatellite diversity is best explained by spread from a single source in the Near East via Anatolia during the Neolithic. Taken with evidence on the origins of other haplogroups, this indicates that most European Y chromosomes originate in the Neolithic expansion. This reinterpretation makes Europe a prime example of how technological and cultural change is linked with the expansion of a Y-chromosomal lineage, and the contrast of this pattern with that shown by maternally inherited mitochondrial DNA suggests a unique role for males in the transition.
Introduction:
Events underlying the distribution of genetic diversity among modern European populations have been the subject of intense debate since the first genetic data became available[1]. Anatomically modern humans, originating in East Africa, colonized Europe from the Near East ∼40 thousand years ago( KYA), then during the last glacial maximum populations retreated into the peninsulas of Iberia, Italy, and the Balkans, followed by northward recolonization from these refugia ∼14 KYA. The most important cultural transition was the adoption of agriculture originating in the Fertile Crescent in the Near East at the start of the Neolithic, ∼10 KYA[2]. It spread rapidly westwards via Anatolia[3]( Figure 1A), reaching Ireland by 6 KYA, accompanied by the development of sedentary populations and demographic expansion. Debate has focused on whether this spread was due to the movement and expansion of Near-Eastern farmers( demic diffusion), or to the transmission of cultural innovation to existing populations( acculturation), who then themselves expanded. The observation of southeast–northwest frequency clines for “classical” genetic markers[1],[4], autosomal DNA markers[5],[6], and Y-chromosomal markers[7],[8]( though not for mitochondrial DNA[mtDNA][9]) has been used to support the demic diffusion model. No dates can be automatically attached to these clines, however, and some[1], detected by principal component analysis, may simply reflect isolation by distance[10]. The direction of movement underlying a cline can also be ambiguous: the high-frequency pole could indicate the area of preexisting substrate least affected by a migration originating far away, or the final destination of a wave of migration into thinly populated territory, where expansion and drift have had their greatest effects[11]. The origins of a frequency cline of a lineage can be illuminated by analysing the diversity within it. For Y-chromosomal lineages defined by binary markers( haplogroups), this can be done using multiple microsatellites. This approach has been applied to haplogroups E, J[12], and I[13] within Europe, but the major western European lineage has not yet been focused upon. The frequency of the major western European lineage, haplogroup( hg) R1b1b2, follows a cline from 12% in Eastern Turkey to 85% in Ireland( Figure 1B), and is currently carried by some 110 million European men. Previous studies of lineages approximately equivalent to hgR1b1b2[7],[8] suggested that it has a Paleolithic origin, based simply on its high frequency in the west. Here, in contrast, we show that the geographical distribution of diversity within the haplogroup is best explained by its spread from a single source from the Near East via Anatolia during the Neolithic. Taken together with the evidence on the origins of many other European haplogroups, this indicates that the great majority of the Y chromosomes of Europeans have their origins in the Neolithic expansion.
Discussion:
Previous observations of the east–west clinal distribution of the common Western European hgR1b1b2( or its equivalent)[7],[8] considered it to be part of a Paleolithic substrate into which farmers from the Near East had diffused. Later analyses have also considered variance, and have conformed to the Paleolithic explanation[14],[15]. Here, we concur that the cline results from demic diffusion, but our evidence supports a different interpretation: that R1b1b2 was carried as a rapidly expanding lineage from the Near East via Anatolia to the western fringe of Europe during the Neolithic. Such mutations arising at the front of a wave of expansion have a high probability of surviving and being propagated, and can reach high frequencies far from their source[11]. Successive founder effects at the edge of the expansion wave can lead to a reduction in microsatellite diversity, even as the lineage increases in frequency. The innovations in the Near East also spread along the southern shore of the Mediterranean, reflected in the expansion of hgE1b1b1b( E-M81)[16], which increases in frequency and reduces in diversity from east to west. In sub-Saharan Africa, hgE1b1a( E-M2) underwent a massive expansion associated with the Bantu expansion[17],[18]. In India, the spread of agriculture has been associated with the introduction of several Y lineages[19], and in Japan, lineages within hgO spread with the Yayoi migration[20], which brought wet rice agriculture to the archipelago. On a more recent timescale, the expansion of the Han culture in China has been linked to demic diffusion[21]. In this context, the apparently low contribution of incoming Y chromosomes to the European Neolithic, despite its antiquity and impact, has appeared anomalous. Our interpretation of the history of hgR1b1b2 now makes Europe a prime example of how expansion of a Y-chromosomal lineage tends to accompany technological and cultural change. Other lineages also show evidence of European Neolithic expansion, hgE1b1b1( E-M35) and hgJ, in particular[12]. Indeed, hgI is the only major lineage for which a Paleolithic origin is generally accepted, but it comprises only 18% of European Y chromosomes[13]. The Basques contain only 8%–20% of this lineage, but 75%–87% hgR1b1b2( Table S1); our findings therefore challenge their traditional “Mesolithic relict” status, and in particular, their use as a proxy for a Paleolithic parental population in admixture modelling of European Y-chromosomal prehistory[22]. Is the predominance of Neolithic-expansion lineages among Y chromosomes reflected in other parts of the genome? Mitochondrial DNA diversity certainly presents a different picture: no east–west cline is discernible, most lineages have a Paleolithic TMRCA[23], and hgH[24] and hgV[25] show signatures of postglacial expansion from the Iberian peninsula. Demic diffusion involves both females and males, but the disparity between mtDNA and Y-chromosomal patterns could arise from an increased and transmitted reproductive success for male farmers compared to indigenous hunter-gatherers, without a corresponding difference between females from the two groups. This would lead to the expansion of incoming Y lineages—as suggested by the high growth rate observed for hgR1b1b2. Similar conclusions have been reached for the Bantu expansion( in which the current Bantu-speaking populations carry many mtDNA lineages originating from hunter-gatherers[26]), the introduction of agriculture to India[19] and the Han expansion[21]. Some studies have found evidence of east–west clines for autosomal loci[6],[27]. By contrast, recent genome-wide SNP typing surveys[28]–[30] find a basic south–north division or gradient, including greater diversity in the south, but they provide no indication of the time-depth of the underlying events, which could in principle involve contributions from the original colonization, postglacial Paleolithic recolonization, Neolithic expansion, and later contact between Africa and southern Europe[31]. The distinction between the geographical patterns of variation of the Y chromosome and those of mtDNA suggest sex-specific factors in patterning European diversity, but the rest of the genome has yet to reveal definitive information. Detailed studies of X-chromosomal and autosomal haplotypes promise to further illuminate the roles of males and females in prehistory.
Arguably the most important cultural transition in the history of modern humans was the development of farming , since it heralded the population growth that culminated in our current massive population size . The genetic diversity of modern populations retains the traces of such past events , and can therefore be studied to illuminate the demographic processes involved in past events . Much debate has focused on the origins of agriculture in Europe some 10 , 000 years ago , and in particular whether its westerly spread from the Near East was driven by farmers themselves migrating , or by the transmission of ideas and technologies to indigenous hunter-gatherers . This study examines the diversity of the paternally inherited Y chromosome , focusing on the commonest lineage in Europe . The distribution of this lineage , the diversity within it , and estimates of its age all suggest that it spread with farming from the Near East . Taken with evidence on the origins of other lineages , this indicates that most European Y chromosomes descend from Near Eastern farmers . In contrast , most maternal lineages descend from hunter-gatherers , suggesting a reproductive advantage for farming males over indigenous hunter-gatherer males during the cultural transition from hunting-gathering to farming .