Southwest Asia and Europe
This is the classic area for debate over cultural versus demic diffusion models for the spread of farming. The original demic diffusion model of Ammerman and CavalliSforza required active population growth along an expanding frontier, moving across Europe from southeast to northwest at an average rate of one kilometer per annum and incorporating indigenous hunter-gatherer populations along the way. Principal components analysis of the genetic data suggested that this particular movement, the major one of three identified in the data, accounted for about 30 percent of the genetic variation in modern European populations (Figure 11.1 upper left).
This model has spawned enormous debate over the past 20 years, most fairly inconclusive until the eruption of mtDNA analysis during the mid-1990s. Alan Fix (1999) has recently suggested that the major southeast-to-northwest dine identified by Cavalli-Sforza and his colleagues, especially in terms of HLA genes, could reflect the effects of selection caused by the farming economy itself, for instance through the associated spread of diseases originating from domesticated animals (zoonotic diseases), or the spread of malaria amongst relatively large and densely settled Neolithic populations, even in temperate latitudes. He does not rule out demic diffusion as a significant process in the genetic foundations of Neolithic Europe, but feels instead that genetic data cannot really illuminate its significance. Cavalli-Sforza himself, supported strongly by Italian geneticist Guido Barbujani and other colleagues, feels conversely that the observed cline is so complex that it must result to a degree from population movement rather than natural selection alone (Cavalli-Sforza and CavalliSforza 1995:149; Barbujani et al. 1998). Other critics, however, point out that the cline is not in itself dateable to any particular period in time, and could just as well be Paleolithic as Neolithic in origin.
The debate has become more lively in recent years with the increasing emphasis on the analysis of haploid markers in mitochondrial DNA and on the Y-chromosome. Interpretations of the data have become complex and varied in the extreme, but two schools of historical interpretation appear to be
consolidating. One, basing its historical reconstructions on the phylogenetic analysis of mtDNA and Y-chromosome lineages, regards most modem Europeans as having essentially local Paleolithic ancestries, with input of Southwest Asian genes during the Neolithic accounting for very little of the modern patterning. This school favors cultural rather than demic diffusion, and its views have most recently been summarized by Martin Richards (2003). The strongest opposed viewpoint favoring demic diffusion derives from modeling the consequences of admixture between postulated Paleolithic European and Neolithic Southwest Asian gene pools, using both the non-recombining systems as well as nuclear DNA.
In order to put this debate into perspective I will review some of the most significant recent opinions in chronological order, subsequent to the classic 1984 study by Ammerman and Cavalli-Sforza. In 1991, a genetic distance analysis of 26 polymorphic genetic systems by Sokal, Oden, and Wilson resulted in the statement: "We conclude that the spread of agriculture through Europe was not simply a case of cultural diffusion, but involved significant differential reproduction of the new farmers whose origins can be traced to the Near East." Full support was given to theories of linked Neolithic and IndoEuropean spreads across Europe, and allowance was made for "diffusive gene flow between the neolithic farmers and mesolithic groups."
Figure 11.1 Upper left: The clinal distribution of markers in 91 nuclear genetic systems from southwest to northwest across Europe, identified by principal components analysis. This is the first principal component within the data and it accounts for about 30% of the total variation. After Cavalli-Sforza and Minch 1997. Upper right: A plot of the most probable Neolithic contribution to the modern Y chromosome genotype, as assessed by Chihki et al. 2002 for European
genetic samples against their geographic distance from the Levant. After Bentley et al. 2003. Lower: A model for Mesolithic-Neolithic genetic admixture in Europe based on demographic assumptions and the archaeological record. After Lahr et al. 2000.
Although Sokal and his team qualified their conclusions in the following year (Sokal et al. 1992), the demic diffusion model for Neolithic and Indo-European spread was soon given further support from a spatial autocorrelation analysis of genetic and linguistic similarities among Eurasian populations by Guido Barbujani and colleagues (1994). Alberto Piazza and colleagues (1995) then used synthetic genetic maps to claim, in agreement with Luca Cavalli-Sforza, that a Neolithic spread through Europe from Southwest Asia accounted for 26 percent of modern genetic variation.
In 1995, Sokal teamed up with Barbujani to return to the issue of demic diffusion, concluding from a computer simulation of five models of microevolution in European populations that: "The genetic structure of current populations speaking IndoEuropean languages seems therefore to largely reflect a Neolithic expansion ... Allele-frequency gradients among Indo-European speakers may be due either to incomplete admixture between dispersing farmers, who presumably spoke IndoEuropean, and pre-existing hunters and gatherers (as in the traditional demic diffusion hypothesis), or to founder effects during the farmers' dispersal" (Barbujani et al. 1995:109). The demic diffusion model was becoming well established.
Indeed, by 1996, an unbiased observer might have drawn the conclusion that demic diffusion had won the day, at least for Neolithic Europe. However, the cultural diffusion school was clearly not going to give in quietly. Martin Richards and colleagues, basing their views on molecular clock calculations and patterns of internal phylogenetic diversity in mtDNA lineages, concluded that "the major extant [mtDNA] lineages throughout Europe predate the Neolithic expansion and ... the spread of agriculture was a substantially indigenous development accompanied by only a relatively minor component of contemporary Middle Eastern agriculturalists" (Richards et al. 1996:185).
Debate naturally ensued over this paper, and battle lines started to emerge (CavalliSforza and Minch 1997: Richards et al. 1997; Barbujani et al. 1998).
The Richards team restated the value of a phylogeographic approach focused on molecular ages for MtDNA lineages, whereas the Barbujani team countered (1998:489): "We do not think that the age of a group of [mtDNA] haplotypes can be mechanically equated to the age of the population from which they came, especially if these haplotypes are also found elsewhere ... inferences from population history must be based on measures of genetic diversity between populations, not between molecules."
In 1998, Antonio Torroni and colleagues entered the debate on the side of the cultural diffusionists, by suggesting that most European mtDNA lineages spread with ancestral populations emerging from late glacial refugia, particularly from Iberia. They claimed also that Southwest Asian mtDNA haplogroup H accounted for between 40 and 60 percent of mtDNA lineages in western Europe, but removed this from Neolithic consideration by giving it an age of more than 25,000 years.
Cultural (non-demic) diffusion received another boost when Bryan Sykes (1999a) restated that the Southwest Asian contribution to the European mtDNA pool was only between 20 and 30 percent, and further claimed that 70 percent of the European mtDNA gene pool originated in the post-glacial re-peopling of Europe, between 11,000 and 14,000 years ago. Martin Richards and colleagues (2000) then restated the case for a Paleolithic inheritance using what they termed "founder analysis," reemphasizing that most European mtDNA lineages expanded after the last glaciation and that under 25 percent of the modem mtDNA pool in Europe was brought in during the Neolithic. However, they remained open to debate on these issues, concurring that: "it is important to bear in mind that these values indicate the likely contribution of each prehistoric expansion to the composition of the present-day mtDNA pool. Extrapolating from this information to details of the demography at the time of the migration, although of course highly desirable for the reconstruction of archaeological processes, is unlikely to be straightforward" (Richards et al. 2000:1272).
In 2000, Ornella Semino and colleagues brought Y-chromosome data into the fray, suggesting that about 78 percent of European Y-chromosome variation related to Paleolithic expansions from glacial refugia in Iberia and Ukraine. They attributed about 22 percent of the modem variation to four haplotypes that spread during the Neolithic from the Levant, thus supporting the claims by Richards and Sykes for only a low Neolithic contribution based on mtDNA.
Between 1996 and 2000, therefore, cultural diffusion was making a strong comeback, even though the percentages actually offered by each school for the Neolithic contribution to the overall European gene pool overlapped considerably, generally between 20 and 30 percent. However, the demic diffusion school was not slow to reply. Lounes Chikhi and colleagues (1998a, 1998b) identified a cline across Europe in molecular DNA markers that paralleled closely the original cline in classical protein markers proposed by Cavalli-Sforza and Piazza. Their own molecular clock calculations placed the population expansion that led to this cline squarely in the Neolithic, and they argued for younger dates for the so-called Paleolithic mtDNA lineages.
Zoe Rosser and colleagues (2000) then indicated clines in two Y-chromosome haplogroups that today account for 45 percent of European variation. These clines were stated, slightly cautiously since they are also strongly influenced by geography, to be good evidence for significant demic diffusion of Neolithic farmers from Southwest Asia. The authors suggested that much of the genetic patterning in Europe may have developed with the spread of Indo-European languages (see also Simoni et al. 2000).
By 2001, Y-chromosome data were sufficiently detailed for Peter Underhill and colleagues (2001a; Underhill 2003) to summarize worldwide patterns, showing that European and west/central Asian populations are closely related in terms of Y haplogroups, particularly when compared to sub-Saharan African and East Asian populations. Two of the Y haplogroups concerned, III and part of VI, could have spread into Europe by Neolithic expansion, and it was acknowledged that the Y-chromosome data support the model of demic diffusion with population admixture, from southeast to northwest across Neolithic Europe.
In 2002, Lounes Chikhi and colleagues analyzed 22 binary markers on the Ychromosome in order to model situations of admixture, followed by genetic drift, between two "ideal" populations, one using modern Near Eastern samples to represent a "Neolithic" mode, the other using Basque and Sardinian samples to represent a "Paleolithic" mode. An essential assumption here is that the real genetic patterning present in the Near East and western Europe 10,000 years ago is unknowable, so only a modeling process of this type will lead to realistic conclusions. The authors concluded that the Neolithic contribution to modern
European Y-chromosomes must have been about 50 percent on average, far higher than either the original estimate by Cavalli-Sforza or that from the mtDNA phylogeographic approach of Martin Richards (both under 30 percent). There is geographical variation, however, with a Near Eastern component of 85-100 percent in southeastern Europe, but only 15-30 percent in France (Figure 11.1 upper right).
By 2002, the supporters of both cultural and demic diffusion had fired many salvos, and the debate is far from over. In 2003, as I finalize this chapter, a compilation of genetics papers on Europe has just been published by the McDonald Institute, as part of a worldwide review of the farming/ language dispersal hypothesis (Bellwood and Renfrew 2003). Guido Barbujani and Isabelle Dupanloup, together with Luca CavalliSforza, and Lounes Chikhi, restate the case for significant demic diffusion of a Southwest Asian Neolithic population into Europe. Barbujani and Dupanloup note how the results of admixture between farmers and foragers will vary in terms of just when in the historical sequence the interbreeding became significant; in other words, foragers would have had far greater genetic impact if they interbred early on with small groups of expanding farmers, much greater than if they went into an early isolationist mode and only emerged much later on to face a farmer population increased by several generations of rapid internal population growth. They conclude "At present, we think there are good reasons to take sides with the earlier (Ammerman and Cavalli-Sforza 1984) rather than with the later (Semino et al. 2000) studies by CavalliSforza's group, and to maintain that a large fraction of the European gene pool is derived from the genes of ancestors who did not live in Europe, but in the Levant, until the Neolithic" (Barbujani and Dupanloup 2003:430).
From the cultural diffusion perspective, Martin Richards and colleagues in the same volume restate the case for only a low proportion of Near Eastern genes across Europe, in fact only about 20 percent, but they also suggest that when the small numbers of Near Eastern farmers did move, they moved far and rapidly. They (2003:464) conclude that "Farming dispersal models may yet have a role to play in explaining language expansions. But grand syntheses based on demic diffusion and the wave of advance, in which farming, languages and genes all expand together, should become a thing of the past." I could not agree more, and sense from this statement a desire for a middle ground.
The middle ground will perhaps be found after more careful consideration of the obvious fact that Europe cannot be considered a single "place" for purposes of Mesolithic to Neolithic transition models. Whatever overall percentage of genes the Neolithic farmers brought into Europe, the actual results of farmerforager interbreeding must have varied across the continent, with the Southwest Asian component necessarily being largest in the south and east, and smallest in the west and north. This has come more into focus with a paper by Roy King and Peter Underhill (2002), in which it is claimed that there are very significant correlations between the distributions of painted pottery and anthropomorphic figurines in Neolithic archaeological contexts in the Levant, Anatolia, and southeastern Europe, and the distribution of a particular Y-chromosome haplogroup termed Eu9. This correlation supports a hypothesis of demic diffusion, at least of males, out of Southwest Asia to as far west as southern France. In addition, analysis of ancient bone from LBK contexts in France and Germany has indicated the presence of mtDNA lineages of Southwest Asian origin - direct evidence for the movement of at least some females during the Neolithic (Jones 2001:161).
As in the earlier Archaeogenetics volume produced by the McDonald Institute (Renfrew and Boyle 2000), the debate over demic vs. cultural diffusion for Neolithic Europe still remains very lively. The dust has not settled yet and there is no obvious neat and tidy genetic reconstruction for the whole of Europe that can be presented in a nutshell. This being the case, can we extract any useful data, independently of the genetics, from the results of skeletal analysis and observations of visible biological characters?
The most obvious example of the latter is the cline in hair and eye pigmentation that runs from relatively dark in the Levant and along the Mediterranean, to light (fair hair, blue eyes) around the North and Baltic Seas and in Scandinavia (Sidrys 1996). At first sight, this could indicate a relative isolation of northern Europeans from any Levantine or Mediterranean influence, but the situation is not really so simple. Natural selection for pale pigmentation via Vitamin D synthesis over a period of 6,000 years, in cold climate circumstances where humans covered themselves with clothing, together with assortative mating, could in theory also have produced the observed cline.
Paleodemographic data also have a contribution to make. An age-at-death
analysis of skeletons in European Neolithic cemeteries has recently allowed Jean-Pierre Bocquet-Appel (2002) to suggest a rapid increase in birth rate immediately following the adoption or spread of agriculture in Europe, followed much later by a rising mortality rate. The earliest farmers were clearly fertile, and Bocquet-Appel draws the conclusion: "With the data currently available, this [pan-European Mesolithic to Neolithic] transition is characterized by a clear rupture with the previous stationary regime of foragers over a period of some 500 years." However, farmer fecundity need not automatically mean demic diffusion of pre-existing farmers, since foragers can also adopt farming and lessen their birth intervals. Bocquet-Appel's results only underpin the reality of rapid early farmer demographic growth.
Another source of skeletal data involves metric and morphological analysis of crania from ancient cemeteries and other archaeological contexts in order to determine population affinities. Slovimil Vencl (1986) analyzed skeletal evidence from central Europe to suggest a tenfold increase in population numbers from the Mesolithic into the Neolithic, and a complete population replacement across the transition, with hunter-gatherers holding out only in areas sub-optimal for farming. A more recent multivariate analysis of cranial data from Turkey and the Levant, plus southeastern and Mediterranean Europe, suggests three conclusions (Pinhasi and Pluciennik in press):
1.PPNB populations in the Levant and Anatolia were very varied.
2.Southeastern European Neolithic peoples were probably drawn from a central Anatolian Neolithic population represented by the burials from catalhoytik.
3.Mediterranean populations originated from a greater degree of MesolithicNeolithic admixture than those in southeastern Europe.
As the authors point out, these conclusions are more precise geographically than those drawn from genetic analyses, the latter being "of insufficient resolution for regional assessment." Their conclusions are rather similar to those drawn by Marta Lahr and colleagues (2000), based on demographic modeling and the archaeological record. These are shown in Figure 11.1 (lower), and indicate something a little similar to the first principal component of Cavalli-
Sforza, in that there is an obvious cline from Anatolia, through Greece and the Balkans, into central and then Mediterranean and western Europe. A recent strontium isotope analysis of female skeletons from LBK contexts in the Rhineland perhaps tells us how such a cline might have originated, in this case via the in-marrying or capture of non-local (Mesolithic?) females who grew up in, and thus acquired chemical signatures in their bones from, upland areas away from the riverine landscape favored for LBK farming (Bentley et al. 2003).
I have deliberately gone into the European situation in depth because of the vast quantity of data available for that region. Clearly, and despite obvious disagreements, the indications point consistently to a "common sense" scenario that requires a Neolithic population to spread in from the southeast and to gradually "disappear" in a genetic sense as the wave of advance spread toward the northwest. The disagreements relate to the strength of this wave of advance, not to its very existence. The perspective I am offering in this book leads me to believe, with geneticists such as Lounes Chikhi and Guido Barbujani, that the strength of this advance was considerable, and that Mesolithic populations, while contributing genes in a markedly clinal fashion, did not contribute very much to the resulting patterns of archaeology and language in Europe, except in situations where they survived temporarily in relative isolation. For other regions of the world we do not have anywhere near such a density of data, but we also have interesting debates.