The genetic history of Europeans (Pinhasi et al. 2012)

This is a nice paper with extensive references on the topic of European origins. Two of its co-authors, Joachim Burger, and Ron Pinhasi are leading a couple of exciting new ancient DNA projects that will probably flood us with interesting new data in the years to come.

From the paper:

Human evolutionary history includes all the complex demographic, natural selection, and stochastic processes that have shaped our species. Despite the limitations of genetic and archaeological data to inform on all the details of human evolution, they constitute an irreplaceable source of information to appraise the key episodes that are likely to have had major impacts on patterns of genetic, morphological, and cultural variation. When considering AMH in Europe, three such critical periods are apparent: (i) the expansion of AMH out of Africa and their colonization of Europe approximately 45 000 years ago (45 ka), (ii) the last glacial maximum (LGM) and the formation of uninhabitable areas in Europe between 27 and 16 ka, and (iii) the arrival of Neolithic culture in southeast Europe and its spread throughout the rest of the continent between 9 and 5 ka. Here we review genetic evidence describing these major demographic episodes in the context of archaeological and chronological data. 

I have postulated that there was at least one important post-5ka event affecting Europe. But, in order to understand how events played out before 5ka and the present, we must first understand the background of what was taking place in Europe before 5ka.

On the earliest settlement of Europe:

Until recently, the earliest date for the first appearance of AMH in Europe had been set to around 42 to 43 ka solely based on their proposed association with Aurignacian artifacts (Table 1) [5,6]. New direct radiocarbon dates of fossils support this view and indicate that AMH appeared in Europe by 44.2– 41.5 calibrated (cal.) ka BP at Kent’s Cavern in southern England [6] and by 45–43 cal. ka BP in Grotta del Cavallo, Italy [7], whereas Neanderthals did not survive in most of Europe and the Caucasus after 39 cal. ka BP [8,9].

These dates are so close to the MP/UP transition in the Levant (49-46 cal ky BP), with the Aurignacian appearing shortly thereafter in both Central Europe and Italy. It would appear that modern humans swiftly colonized Europe after they made the crucial UP leap. Of course, in my opinion, this population was ultimately descended from inhabitants of Arabia, escaping post-70ka climatic deterioration and pre-100ka with the archaeologically attestedNubian Complex. But, in any case, it is probably the last crucial step, when humans went into warp drive post-50ka that led to the first modern human colonization of Europe and ultimately the extinction (or absorption?) of the Neandertals.

But, the early colonizers were in for a rough patch of climate that last for several millennia, making whole parts of Europe uninhabitable, and allowing few ones to survive in the south of the continent:

After the disappearance of the Neanderthals and particularly during the LGM, the northern parts of Europe were covered by ice sheets, leaving humans to survive in poorly resourced environments [10,11]. Parts of northern Europe were either completely abandoned [12] or sparsely populated [13]. The archaeological record of this period catalogs a complex series of interrelated material cultures that vary in their geographic ranges and temporal durations (Table 1). Spatial patterns of material culture change have been interpreted as indicating colonization of regions up to 52 degrees N latitude during the Gravettian, followed by partial or complete retreat of most northern populations by 24 ka, and recolonization of these regions by 20–16 ka, with some continuity of occupation in more southern latitudes [14]. However, the extent to which material cultures correspond to distinct human populations, and to which their distribu- tion changes through time correspond to demographic pro- cesses, remains unclear. 

The following table presents a very useful summary of archaeological developments in west Eurasia:

So far, we have substantial autosomal data of modern humans only from the Mesolithic onwards (Iberia), but also mtDNA from much older specimens of the Gravettian in Italy and Russia.

Apparently, other people are looking to extract ancient genomic DNA from older remains as well:

A group led by evolutionary geneticist Johannes Krause of the University of Tubingen, Germany, is trying to remove and reassemble nuclear DNA from the bones of roughly 20,000-year-old people in Europe. If successful, that effort will provide the first look at whether Stone Age humans carried more Neandertal genes than people today do. “It’s a completely open question whether more interbreeding occurred in the past than what we’ve found so far,” Krause says.

But, let's see where things stand now.

Ancient mtDNA sequences recovered from three Upper Paleolithic and 14 Mesolithic and Neolithic hunter-gatherers all belong to the mtDNA haplogroup U [48], currently found at frequencies between 1 and 7% in most modern European populations, but at up to 20% in Baltic populations and around 40% in Saami. Interestingly, almost all pre-Neolithic hunter-gatherers from Central and Northeastern Europe sequenced to date, and the majority of European post-Neolithic hunter-gatherers, carry U-type mtDNA [48,49] (Figure 1a,c). There are three exceptions: two Italian individuals with N* and pre-HV types [50], and one from Sweden [46]; the latter dating to the late Neolithic and possibly being the result of an admix- ture event with incoming farmers. In all other hunter- gatherer samples, the now common mtDNA lineages H, T, K, and J are absent, suggesting that these mtDNA lineages were introduced during the Neolithic period. 

The mtDNA evidence is indeed the strongest argument for large-scale population replacement during the Neolithic, a scenario which has found support by the sequencing of Neolithic hunter-gatherers from Gotland Sweden and Mesolithic ones from Iberia.

The authors note that while early farming groups largely lacked mtDNA haplogroup U, the later ones possessed it to some extent:

Maps showing Europe in times slices and depicting the locations from which ancient mitochondrial DNA (mtDNA) sequences were retrieved. Squares represent hunter-gatherer individuals and circles represent farming individuals. Lineages belonging to the U-clade are shown in red. Other lineages are shown in yellow. (a) Paleolithic and Mesolithic hunter-gatherers 13 500–8300 BP (plotted on a map ofEurope during the last glacial maximum ca 22 000 BP).All Pleistocene hunter-gatherers analyzed to date carry mitochondrial lineages that belong to one of the U-clades: U2, U4, or U5. (b) Early farmers 7600–6500 BP. The map illustrates the approximate arrival times and duration of the earliest Neolithic cultures (in years BP). Very few of the early farmers belong to one of the U-clade mtDNA haplotypes, indicating discontinuity between Paleolithic/Mesolithic hunter-gatherers and early farmers [48,64]. (c) Later hunter-gatherers 6500–4500 BP. Whereas early hunter-gatherers carry exclusively mitochondrial U-lineages,later hunter-gatherers show additional lineages that are also present in early farming groups(b), pointing to a possible admixture between the groups or a change in lifestyle of former farmers back to hunting-gathering in Northern Europe. (d) Later farmers 6500–4500 BP. Compared to the period of the first appearance of farmers, late farmers have a significantly higher frequency of U-lineages. This can be explained by increasing rates of admixture between farmer and hunter gatherer groups during this period and by the adoption of a farming lifestyle by hunter-gatherers. The maps are adapted from [69] and show datapoints from [46,48,51, 54–56,61,62,64,70,71]. Abbreviation: BP, before present. 

And, of course, we have the ubiquitous Y-haplogroup G2a as the lineage par excellence of the first European farmers:

In contrast to mtDNA, ancient Y-chromosome data has until recently been less informative, but a single Y-chro-mosome haplotype (G2a) in 20 of 22 male individuals from the Late Neolithic cave site at Treilles [62] led to the hypothesis that a small male founding population arrived in Southern France, probably by a maritime route from the eastern Mediterranean, in the early Neolithic. The same haplotype was also found in five of six individuals from the Avellaner Cave [61] and in one out of three Central Euro-pean LBK individuals [63]. If authentic, the presence of the Y-chromosome haplogroup G2a in 26 of 31 Neolithic individuals from Germany, France, and Spain is both surprising and intriguing, but this requires further examination. 

The only high coverage genome sequence of a prehistoric European individual is that of the Tyrolean Iceman, Oetzi, a 5300 year-old individual from South Tyrol, which was recently reported at 7-fold coverage [45]. Comparison with 1300 contemporary Europeans indicated closest genetic affinities with southern Europeans, particularly inhabi-tants of the Tyrrhenian Islands. Intriguingly, this is also the region where the Y-chromosome haplotype of the Ice-man is found at highest frequency, and this haplotype belongs to the same G2a haplogroup described above.

And of course:

Future research should also reveal the effects of post-Neolithic demographic processes, including migration events, which preliminary data suggest had a major impact upon the distribution of genetic variation. These include events associated with Bronze Age civilizations, Iron Age cultures, and later migrations, including those triggered by the rise and fall of Empires.

The recovery of the European past has only just begun.

Trends in Genetics doi:10.1016/j.tig.2012.06.006

The genetic history of Europeans 

Ron Pinhasi, Mark G. Thomas, Michael Hofreiter, Mathias Currat, Joachim Burger

The evolutionary history of modern humans is characterized by numerous migrations driven by environmental change, population pressures, and cultural innovations. In Europe, the events most widely considered to have had a major impact on patterns of genetic diversity are the initial colonization of the continent by anatomically modern humans (AMH), the last glacial maximum, and the Neolithic transition. For some decades it was assumed that the geographical structuring of genetic diversity within Europe was mainly the result of gene flow during and soon after the Neolithic transition, but recent advances in next-generation sequencing (NGS) technologies, computer simulation modeling, and ancient DNA (aDNA) analyses are challenging this simplistic view. Here we review the current knowledge on the evolutionary history of humans in Europe based on archaeological and genetic data.

Link

Farming Conquered Europe at Least Twice

The rise of agriculture in the Middle East, nearly 11,000 years ago, was a momentous event in human prehistory. But just how farming spread from there into Europe has been a matter of intense research. A new study of ancient DNA from 5000-year-old skeletons found in a French cave suggests that early farmers entered the European continent by at least two different routes and reveals new details about the social structures and dairying practices of some of their societies.

Scientists studying the spread of farming into Europe have numerous questions: Was agriculture brought in primarily by Middle Eastern farmers who replaced the resident hunter-gatherers? Or did agriculture advance through the spread of technology and ideas rather than people? And was there just one wave of farming into the continent or multiple waves and routes?

Until recently, researchers had to rely on the genetic profiles of modern-day Europeans and Middle Easterners for clues. Numerous such studies, especially of Y chromosomes, which are transmitted via the paternal line, suggest that actual farmers, not just their ideas, spread westward over the millennia, eventually reaching the British Isles. Yet other studies, based on mitochondrial DNA (mtDNA), which is inherited maternally, have come to the opposite conclusion, suggesting that farmers had local European ancestry.

Now, new studies have begun to resolve these issues by sequencing the DNA of the prehistoric farmers themselves. Some of this research, most notably in Germany, suggests that male farmers entering central Europe mated with local female hunter-gatherers—thus possibly resolving the contradiction between the Y chromosome and mtDNA results.

The new paper, published online this week in the Proceedings of the National Academy of Sciences, backs up that idea. A team led by molecular anthropologist Marie Lacan of the Paul Sabatier University in Toulouse, France, reports work on ancient DNA—both mitochondrial and Y-chromosomal—from more than two dozen skeletons found in the 1930s in a cave called Treilles in southern France. Archaeologists think Treilles is a communal grave site because the bones add up to 149 individuals, 86 adults and 63 children. The team took DNA in such a way as to ensure that each individual was sampled only once (using teeth that were still attached to a lower jaw) and was able to obtain ancient DNA from 29 people.

They found that the female and male lineages seemed to have different origins. The mtDNA showed genetic markers previously identified as having deep roots in ancient European hunter-gatherer populations, but the Y chromosomes showed the closest affinities to Europeans currently living along the Mediterranean regions of southern Europe, such as Turkey, Cyprus, Portugal, and Italy. The team concludes that, in addition to the spread of farming into Central Europe suggested by the German studies, there appears to have been at least one additional route via southern Europe.

The communal grave also yielded additional intriguing details about these ancient Europeans. Most of the skeletons were males, and many appeared to be very closely related: At least two pairs of individuals were almost certainly father and son, and another pair were brothers. That suggests that the incoming male farmers established a so-called patrilocal society, in which the men stay put on their land but mate with women who come in from surrounding regions, the team concludes.

The study also showed that, in contrast to ancient DNA findings from central Europe, the people from Treilles lacked a key genetic variant that allows the body to digest lactose into adulthood. That’s consistent with other archaeological evidence that central European farmers herded dairy cows, whereas Mediterranean farmers herded sheep and goats and drank fermented milk, which has much lower lactose levels.

Lounès Chikhi, a geneticist at Paul Sabatier University who has studied the spread of farming for many years, praises the team for getting both Y chromosome and mtDNA from the same skeletal collection. “We have been calling for exactly this kind of data,” Chikhi says, “so I am very excited.” Colin Renfrew, an archaeologist at the University of Cambridge in the United Kingdom, agrees that the findings support a second, southern European spread of farming. “They do indeed suggest a significant population influx from the Eastern Mediterranean.”

But Wolfgang Haak, a geneticist at the University of Adelaide in Australia, says that Treilles may be too young to provide reliable information about the spread of farming in southern Europe, which began at least 2000 years earlier. While these earlier migrations “should have left a genetic mark in later periods,” Haak says, Treilles might not be the “best candidate” for tracing them. The ancient DNA Lacan is now extracting from skeletons across France and Spain, Haak says, should provide more “piece[s] of the enormous puzzle we are trying to put together.”

Emerging genetic patterns of the european neolithic

American Journal of Physical Anthropology DOI: 10.1002/ajpa.22074

Emerging genetic patterns of the european neolithic: Perspectives from a late neolithic bell beaker burial site in Germany

Esther J. Lee et al. 

Abstract 

The transition from hunting and gathering to agriculture in Europe is associated with demographic changes that may have shifted the human gene pool of the region as a result of an influx of Neolithic farmers from the Near East. However, the genetic composition of populations after the earliest Neolithic, when a diverse mosaic of societies that had been fully engaged in agriculture for some time appeared in central Europe, is poorly known. At this period during the Late Neolithic (ca. 2,800–2,000 BC), regionally distinctive burial patterns associated with two different cultural groups emerge, Bell Beaker and Corded Ware, and may reflect differences in how these societies were organized. Ancient DNA analyses of human remains from the Late Neolithic Bell Beaker site of Kromsdorf, Germany showed distinct mitochondrial haplotypes for six individuals, which were classified under the haplogroups I1, K1, T1, U2, U5, and W5, and two males were identified as belonging to the Y haplogroup R1b. In contrast to other Late Neolithic societies in Europe emphasizing maintenance of biological relatedness in mortuary contexts, the diversity of maternal haplotypes evident at Kromsdorf suggests that burial practices of Bell Beaker communities operated outside of social norms based on shared maternal lineages. Furthermore, our data, along with those from previous studies, indicate that modern U5-lineages may have received little, if any, contribution from the Mesolithic or Neolithic mitochondrial gene pool. 


LINK

BEAN: Bridging the European and Anatolian Neolithic

The Neolithic first appears outside its core region in the Near East and central Anatolia after 7.000 BC, in the western part of Anatolia. This is a key staging area for the further spread of the Neolithic culture through Europe. The mode and tempo of the spread of the Neolithic remains problematic: although detailed chronologies of Neolithisation exist for individual regions, a precise and comprehensive Neolithisation theory is still needed for the entire area between central Anatolia and central Europe.

Marie Curie International Training Network aims to build a new generation of students able to identify and address the main aspects of this crucial period for the future history of the entire Eurasian continent.The BEAN network focuses on demographic questions surrounding the dissemination of the cultural, technological, and biological components of the Neolithic from western Anatolia and the Balkans to the rest of Europe.  The following are the primary research questions of  Marie Curie International Training Network :

       

1.  To determine the extent to which humans migrated (along with their domesticates) into  new lands during the establishment of the Neolithic in western Anatolia and southeastern Europe.

 2.  To understand the mode and tempo of the change from foraging to farming in the Neolithic of western Anatolia and southeastern Europe and the degree of cultural exchange  between local and migrant populations.

 3.  To reconstruct the patterns of circulation of raw materials, manufactured goods and ideas.

 4. To map the population structure and estimate demographic parameters of the human  groups involved in the transition.

BEAN is a Marie Curie initial training network (ITN). The aim of the BEAN training network is to educate a new generation of researchers that will be able to combine the important aspects of  prehistoric archaeology, palaeodemography, population genetics, biostatistics, and next-generation molecular genetics while developing specialized skills in their particular scientific discipline. The broader question of the Neolithisation of Europe will serve as an intellectual framework structuring the research and training opportunities provided by BEAN network participants. 

The BEAN network proposes to carry out much-needed research into the origins of settled farming life in Europe  and the Europeans themselves while training the next generation of European researchers in the cutting-edge techniques of three different research areas:

                1.       Anthropology and Genetics

                2.       Simulations and Modelling

                3.       Prehistoric Archaeology

These  scientific disciplines reinforce each other to form a robust research framework within which researchers in the BEAN network can approach one of the most pressing archaeological questions of our time: the Neolithisation of Europe.

Simulations and Modelling

Advanced computer models can be used to simulate the diffusion of genes through a population with time, in order to test hypothetical demographic scenarios for the Neolithic transition in Western Anatolia and the Balkans.  These  models can be built using data obtained from archaeological and palaeodemographic research, and evaluated using modern and ancient DNA from populations living in the region.  By altering demographic and biological parameters, alternative hypotheses can be explored. Modelling prehistoric gene flow will enable researchers to better understand the genetic correlates and consequences of the Neolithic transition.

Anthropology and Genetics
Recent advances in the anthropological sciences have made the Neolithisation question much more tractable for modern researchers. With the advent of palaeogenetic methods such as the analysis of DNA from archaeological skeletons, and especially with the possibilities of the next generation sequencing technologies (NGS), new data have become available that now render prehistoric demographic inferences possible. When ancient DNA data are analysed by appropriate statistical inference methods, particularly those applying coalescent theory, a reliable reconstruction of past populations structure is feasible. The increasingly sophisticated methods employed by biological anthropologists to examine the morphology and composition of fossilized tissues have further enhanced the informative potential of ancient human remains.

Cranial variation and the transition to agriculture in Europe

Abstract

Debates surrounding the nature of the Neolithic demographic transition in Europe have historically centred on two opposing models; a 'demic' diffusion model whereby incoming farmers from the Near East and Anatolia effectively replaced or completely assimilated indigenous Mesolithic foraging communities and an 'indigenist' model resting on the assumption that ideas relating to agriculture and animal domestication diffused from the Near East, but with little or no gene flow. The extreme versions of these dichotomous models have been heavily contested primarily on the basis of archaeological and modern genetic data. However, in recent years there has been a growing acceptance of the likelihood that both processes were ongoing throughout the Neolithic transition and that a more complex, regional approach is required to fully understand the change from a foraging to a primarily agricultural mode of subsistence in Europe. Craniometric data have been particularly useful for testing these more complex scenarios, as they can reliably be employed as a proxy for the genetic relationships amongst Mesolithic and Neolithic populations. In contrast, modern genetic data assume that modern European populations accurately reflect the genetic structure of Europe at the time of the Neolithic transition, while ancient DNA data are still not geographically or temporally detailed enough to test continent-wide processes. Here, with particular emphasis on the role of craniometric analyses, we review the current state of knowledge regarding the cultural and biological nature of the Neolithic transition in Europe.

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