Torsten Günther

Genomic Diversity and Admixture Differs for Stone-Age Scandinavian Foragers and Farmers

Hunters and Farmers The Neolithic period in Europe saw the transition from a hunter-gatherer lifestyle to farming. Previous genetic analyses have suggested that hunter-gatherers were replaced by immigrant farmers. Skoglund et al. (p. 747, published online 24 April) sequenced one Mesolithic and nine Neolithic Swedish individuals to examine the transition from hunter-gatherers to farmers. Substantial genetic differentiation was observed between hunter-gatherers and farmers: There was lower genetic diversity within the hunter-gatherers and gene flow from the hunter-gatherers into the farmers but not vice versa. Population dynamics of Scandinavian Mesolithic and Neolithic hunter-gatherers differ from those of early farmers. Prehistoric population structure associated with the transition to an agricultural lifestyle in Europe remains a contentious idea. Population-genomic data from 11 Scandinavian Stone Age human remains suggest that hunter-gatherers had lower genetic diversity than that of farmers. Despite their close geographical proximity, the genetic differentiation between the two Stone Age groups was greater than that observed among extant European populations. Additionally, the Scandinavian Neolithic farmers exhibited a greater degree of hunter-gatherer–related admixture than that of the Tyrolean Iceman, who also originated from a farming context. In contrast, Scandinavian hunter-gatherers displayed no significant evidence of introgression from farmers. Our findings suggest that Stone Age foraging groups were historically in low numbers, likely owing to oscillating living conditions or restricted carrying capacity, and that they were partially incorporated into expanding farming groups.

Ancient genomes link early farmers from Atapuerca in Spain to modern-day Basques

Significance The transition from a foraging subsistence strategy to a sedentary farming society is arguably the greatest innovation in human history. Some modern-day groups—specifically the Basques—have been argued to be a remnant population that connect back to the Paleolithic. We present, to our knowledge, the first genome-wide sequence data from eight individuals associated with archaeological remains from farming cultures in the El Portalón cave (Atapuerca, Spain). These individuals emerged from the same group of people as other Early European farmers, and they mixed with local hunter–gatherers on their way to Iberia. The El Portalón individuals showed the greatest genetic affinity to Basques, which suggests that Basques and their language may be linked with the spread of agriculture across Europe. The consequences of the Neolithic transition in Europe—one of the most important cultural changes in human prehistory—is a subject of great interest. However, its effect on prehistoric and modern-day people in Iberia, the westernmost frontier of the European continent, remains unresolved. We present, to our knowledge, the first genome-wide sequence data from eight human remains, dated to between 5,500 and 3,500 years before present, excavated in the El Portalón cave at Sierra de Atapuerca, Spain. We show that these individuals emerged from the same ancestral gene pool as early farmers in other parts of Europe, suggesting that migration was the dominant mode of transferring farming practices throughout western Eurasia. In contrast to central and northern early European farmers, the Chalcolithic El Portalón individuals additionally mixed with local southwestern hunter–gatherers. The proportion of hunter–gatherer-related admixture into early farmers also increased over the course of two millennia. The Chalcolithic El Portalón individuals showed greatest genetic affinity to modern-day Basques, who have long been considered linguistic and genetic isolates linked to the Mesolithic whereas all other European early farmers show greater genetic similarity to modern-day Sardinians. These genetic links suggest that Basques and their language may be linked with the spread of agriculture during the Neolithic. Furthermore, all modern-day Iberian groups except the Basques display distinct admixture with Caucasus/Central Asian and North African groups, possibly related to historical migration events. The El Portalón genomes uncover important pieces of the demographic history of Iberia and Europe and reveal how prehistoric groups relate to modern-day people.

Genomic Evidence Establishes Anatolia as the Source of the European Neolithic Gene Pool

Anatolia and the Near East have long been recognized as the epicenter of the Neolithic expansion through archaeological evidence. Recent archaeogenetic studies on Neolithic European human remains have shown that the Neolithic expansion in Europe was driven westward and northward by migration from a supposed Near Eastern origin [1-5]. However, this expansion and the establishment of numerous culture complexes in the Aegean and Balkans did not occur until 8,500 before present (BP), over 2,000 years after the initial settlements in the Neolithic core area [6-9]. We present ancient genome-wide sequence data from 6,700-year-old human remains excavated from a Neolithic context in Kumtepe, located in northwestern Anatolia near the well-known (and younger) site Troy [10]. Kumtepe is one of the settlements that emerged around 7,000 BP, after the initial expansion wave brought Neolithic practices to Europe. We show that this individual displays genetic similarities to the early European Neolithic gene pool and modern-day Sardinians, as well as a genetic affinity to modern-day populations from the Near East and the Caucasus. Furthermore, modern-day Anatolians carry signatures of several admixture events from different populations that have diluted this early Neolithic farmer component, explaining why modern-day Sardinian populations, instead of modern-day Anatolian populations, are genetically more similar to the people that drove the Neolithic expansion into Europe. Anatolias central geographic location appears to have served as a connecting point, allowing a complex contact network with other areas of the Near East and Europe throughout, and after, the Neolithic.

The Demographic Development of the First Farmers in Anatolia

Summary The archaeological documentation of the development of sedentary farming societies in Anatolia is not yet mirrored by a genetic understanding of the human populations involved, in contrast to the spread of farming in Europe [1, 2, 3]. Sedentary farming communities emerged in parts of the Fertile Crescent during the tenth millennium and early ninth millennium calibrated (cal) BC and had appeared in central Anatolia by 8300 cal BC [4]. Farming spread into west Anatolia by the early seventh millennium cal BC and quasi-synchronously into Europe, although the timing and process of this movement remain unclear. Using genome sequence data that we generated from nine central Anatolian Neolithic individuals, we studied the transition period from early Aceramic (Pre-Pottery) to the later Pottery Neolithic, when farming expanded west of the Fertile Crescent. We find that genetic diversity in the earliest farmers was conspicuously low, on a par with European foraging groups. With the advent of the Pottery Neolithic, genetic variation within societies reached levels later found in early European farmers. Our results confirm that the earliest Neolithic central Anatolians belonged to the same gene pool as the first Neolithic migrants spreading into Europe. Further, genetic affinities between later Anatolian farmers and fourth to third millennium BC Chalcolithic south Europeans suggest an additional wave of Anatolian migrants, after the initial Neolithic spread but before the Yamnaya-related migrations. We propose that the earliest farming societies demographically resembled foragers and that only after regional gene flow and rising heterogeneity did the farming population expansions into Europe occur.

Southern African ancient genomes estimate modern human divergence to 350,000 to 260,000 years ago

Ancient DNA pushes human emergence back Anatomically modern humans evolved in Africa, but pinpointing when has been difficult. Schlebusch et al. sequenced three ancient African genomes from the Stone Age, about 2000 years old, and four from the Iron Age, 300 to 500 years old. One of the oldest samples, sequenced to 13× coverage, appears most closely to resemble individuals from the present-day San population. However, this individual seems to have lacked genetic contributions from other modern African populations, including pastoralists and farmers, which were observed in modern San individuals. Thus, the earliest divergence between human populations may have occurred 350,000 to 260,000 years ago. Science, this issue p. 652 Ancient African genomes push back the timing of the split between human populations. Southern Africa is consistently placed as a potential region for the evolution of Homo sapiens. We present genome sequences, up to 13x coverage, from seven ancient individuals from KwaZulu-Natal, South Africa. The remains of three Stone Age hunter-gatherers (about 2000 years old) were genetically similar to current-day southern San groups, and those of four Iron Age farmers (300 to 500 years old) were genetically similar to present-day Bantu-language speakers. We estimate that all modern-day Khoe-San groups have been influenced by 9 to 30% genetic admixture from East Africans/Eurasians. Using traditional and new approaches, we estimate the first modern human population divergence time to between 350,000 and 260,000 years ago. This estimate increases the deepest divergence among modern humans, coinciding with anatomical developments of archaic humans into modern humans, as represented in the local fossil record.

Ancient X chromosomes reveal contrasting sex bias in Neolithic and Bronze Age Eurasian migrations

Significance Studies of differing female and male demographic histories on the basis of ancient genomes can provide insight into the social structures and cultural interactions during major events in human prehistory. We consider the sex-specific demography of two of the largest migrations in recent European prehistory. Using genome-wide ancient genetic data from multiple Eurasian populations spanning the last 10,000 years, we find no evidence of sex-biased migrations from Anatolia, despite the shift to patrilocality associated with the spread of farming. In contrast, we infer a massive male-biased migration from the steppe during the late Neolithic and Bronze Age. The contrasting patterns of sex-specific migration during these two migrations suggest that different sociocultural processes drove the two events. Dramatic events in human prehistory, such as the spread of agriculture to Europe from Anatolia and the late Neolithic/Bronze Age migration from the Pontic-Caspian Steppe, can be investigated using patterns of genetic variation among the people who lived in those times. In particular, studies of differing female and male demographic histories on the basis of ancient genomes can provide information about complexities of social structures and cultural interactions in prehistoric populations. We use a mechanistic admixture model to compare the sex-specifically–inherited X chromosome with the autosomes in 20 early Neolithic and 16 late Neolithic/Bronze Age human remains. Contrary to previous hypotheses suggested by the patrilocality of many agricultural populations, we find no evidence of sex-biased admixture during the migration that spread farming across Europe during the early Neolithic. For later migrations from the Pontic Steppe during the late Neolithic/Bronze Age, however, we estimate a dramatic male bias, with approximately five to 14 migrating males for every migrating female. We find evidence of ongoing, primarily male, migration from the steppe to central Europe over a period of multiple generations, with a level of sex bias that excludes a pulse migration during a single generation. The contrasting patterns of sex-specific migration during these two migrations suggest a view of differing cultural histories in which the Neolithic transition was driven by mass migration of both males and females in roughly equal numbers, perhaps whole families, whereas the later Bronze Age migration and cultural shift were instead driven by male migration, potentially connected to new technology and conquest.

Population genomics of Mesolithic Scandinavia: Investigating early postglacial migration routes and high-latitude adaptation

Scandinavia was one of the last geographic areas in Europe to become habitable for humans after the Last Glacial Maximum (LGM). However, the routes and genetic composition of these postglacial migrants remain unclear. We sequenced the genomes, up to 57× coverage, of seven hunter-gatherers excavated across Scandinavia and dated from 9,500–6,000 years before present (BP). Surprisingly, among the Scandinavian Mesolithic individuals, the genetic data display an east–west genetic gradient that opposes the pattern seen in other parts of Mesolithic Europe. Our results suggest two different early postglacial migrations into Scandinavia: initially from the south, and later, from the northeast. The latter followed the ice-free Norwegian north Atlantic coast, along which novel and advanced pressure-blade stone-tool techniques may have spread. These two groups met and mixed in Scandinavia, creating a genetically diverse population, which shows patterns of genetic adaptation to high latitude environments. These potential adaptations include high frequencies of low pigmentation variants and a gene region associated with physical performance, which shows strong continuity into modern-day northern Europeans.

Genomic and phenotypic differentiation of Arabidopsis thaliana along altitudinal gradients in the North Italian Alps.

Altitudinal gradients in mountain regions are short‐range clines of different environmental parameters such as temperature or radiation. We investigated genomic and phenotypic signatures of adaptation to such gradients in five Arabidopsis thaliana populations from the North Italian Alps that originated from 580 to 2350 m altitude by resequencing pools of 19–29 individuals from each population. The sample includes two pairs of low‐ and high‐altitude populations from two different valleys. High‐altitude populations showed a lower nucleotide diversity and negative Tajimas D values and were more closely related to each other than to low‐altitude populations from the same valley. Despite their close geographic proximity, demographic analysis revealed that low‐ and high‐altitude populations split between 260 000 and 15 000 years before present. Single nucleotide polymorphisms whose allele frequencies were highly differentiated between low‐ and high‐altitude populations identified genomic regions of up to 50 kb length where patterns of genetic diversity are consistent with signatures of local selective sweeps. These regions harbour multiple genes involved in stress response. Variation among populations in two putative adaptive phenotypic traits, frost tolerance and response to light/UV stress was not correlated with altitude. Taken together, the spatial distribution of genetic diversity reflects a potentially adaptive differentiation between low‐ and high‐altitude populations, whereas the phenotypic differentiation in the two traits investigated does not. It may resemble an interaction between adaptation to the local microhabitat and demographic history influenced by historical glaciation cycles, recent seed dispersal and genetic drift in local populations.

Estimating genetic kin relationships in prehistoric populations

Archaeogenomic research has proven to be a valuable tool to trace migrations of historic and prehistoric individuals and groups, whereas relationships within a group or burial site have not been investigated to a large extent. Knowing the genetic kinship of historic and prehistoric individuals would give important insights into social structures of ancient and historic cultures. Most archaeogenetic research concerning kinship has been restricted to uniparental markers, while studies using genome-wide information were mainly focused on comparisons between populations. Applications which infer the degree of relationship based on modern-day DNA information typically require diploid genotype data. Low concentration of endogenous DNA, fragmentation and other post-mortem damage to ancient DNA (aDNA) makes the application of such tools unfeasible for most archaeological samples. To infer family relationships for degraded samples, we developed the software READ (Relationship Estimation from Ancient DNA). We show that our heuristic approach can successfully infer up to second degree relationships with as little as 0.1x shotgun coverage per genome for pairs of individuals. We uncover previously unknown relationships among prehistoric individuals by applying READ to published aDNA data from several human remains excavated from different cultural contexts. In particular, we find a group of five closely related males from the same Corded Ware culture site in modern-day Germany, suggesting patrilocality, which highlights the possibility to uncover social structures of ancient populations by applying READ to genome-wide aDNA data. READ is publicly available from https://bitbucket.org/tguenther/read.

Ancient genomes from southern Africa pushes modern human divergence beyond 260,000 years ago

Southern Africa is consistently placed as one of the potential regions for the evolution of Homo sapiens. To examine the region’s human prehistory prior to the arrival of migrants from East and West Africa or Eurasia in the last 1,700 years, we generated and analyzed genome sequence data from seven ancient individuals from KwaZulu-Natal, South Africa. Three Stone Age hunter-gatherers date to ~2,000 years ago, and we show that they were related to current-day southern San groups such as the Karretjie People. Four Iron Age farmers (300–500 years old) have genetic signatures similar to present day Bantu-speakers. The genome sequence (13x coverage) of a juvenile boy from Ballito Bay, who lived ~2,000 years ago, demonstrates that southern African Stone Age hunter-gatherers were not impacted by recent admixture; however, we estimate that all modern-day Khoekhoe and San groups have been influenced by 9–22% genetic admixture from East African/Eurasian pastoralist groups arriving >1,000 years ago, including the Ju|‘hoansi San, previously thought to have very low levels of admixture. Using traditional and new approaches, we estimate the population divergence time between the Ballito Bay boy and other groups to beyond 260,000 years ago. These estimates dramatically increases the deepest divergence amongst modern humans, coincide with the onset of the Middle Stone Age in sub-Saharan Africa, and coincide with anatomical developments of archaic humans into modern humans as represented in the local fossil record. Cumulatively, cross-disciplinary records increasingly point to southern Africa as a potential (not necessarily exclusive) ‘hot spot’ for the evolution of our species.