Helena Malmström

Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe.

Farmer Displaced European Hunters Our understanding of prehistoric demography and human evolution has been improved by analysis of ancient DNA. Skoglund et al. (p. 466) describe the retrieval and analysis of genomic DNA from ancient (~5000-year-old) northern European Neolithic individuals within modern Sweden. These include three hunter-gatherers from the Pitted Ware Culture horizon and one farmer ascribed to the Mid-Neolithic North-Central TRB culture. The hunter-gatherers displayed a distinct genetic signature, similar to that of extant northern Europeans, whereas the farmers genetic signature more closely resembled southern Europeans, suggesting migration and admixture during the spread of farming. Genomic analysis of ancient Scandinavians reveals that agricultural expansion was driven by long-range population movement. The farming way of life originated in the Near East some 11,000 years ago and had reached most of the European continent 5000 years later. However, the impact of the agricultural revolution on demography and patterns of genomic variation in Europe remains unknown. We obtained 249 million base pairs of genomic DNA from ~5000-year-old remains of three hunter-gatherers and one farmer excavated in Scandinavia and find that the farmer is genetically most similar to extant southern Europeans, contrasting sharply to the hunter-gatherers, whose distinct genetic signature is most similar to that of extant northern Europeans. Our results suggest that migration from southern Europe catalyzed the spread of agriculture and that admixture in the wake of this expansion eventually shaped the genomic landscape of modern-day Europe.

Ancient DNA Reveals Lack of Continuity between Neolithic Hunter-Gatherers and Contemporary Scandinavians

The driving force behind the transition from a foraging to a farming lifestyle in prehistoric Europe (Neolithization) has been debated for more than a century [1-3]. Of particular interest is whether population replacement or cultural exchange was responsible [3-5]. Scandinavia holds a unique place in this debate, for it maintained one of the last major hunter-gatherer complexes in Neolithic Europe, the Pitted Ware culture [6]. Intriguingly, these late hunter-gatherers existed in parallel to early farmers for more than a millennium before they vanished some 4,000 years ago [7, 8]. The prolonged coexistence of the two cultures in Scandinavia has been cited as an argument against population replacement between the Mesolithic and the present [7, 8]. Through analysis of DNA extracted from ancient Scandinavian human remains, we show that people of the Pitted Ware culture were not the direct ancestors of modern Scandinavians (including the Saami people of northern Scandinavia) but are more closely related to contemporary populations of the eastern Baltic region. Our findings support hypotheses arising from archaeological analyses that propose a Neolithic or post-Neolithic population replacement in Scandinavia [7]. Furthermore, our data are consistent with the view that the eastern Baltic represents a genetic refugia for some of the European hunter-gatherer populations.

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.

The genetic prehistory of the New World Arctic

Introduction Humans first peopled the North American Arctic (northern Alaska, Canada, and Greenland) around 6000 years ago, leaving behind a complex archaeological record that consisted of different cultural units and distinct ways of life, including the Early Paleo-Eskimos (Pre-Dorset/Saqqaq), the Late Paleo-Eskimos (Early Dorset, Middle Dorset, and Late Dorset), and the Thule cultures. Genetic origins of Paleo-Eskimos and Neo-Eskimos. All Paleo-Eskimos represent a single migration pulse from Siberia into the Americas, independent of the Neo-Eskimo Thule people (ancestors of modern-day Inuit) and the related extinct Sadlermiut population. The Siberian Birnirk people were likely cultural and genetic ancestors of modern-day Inuit. We also show ancient admixture between the Paleo- and Neo-Eskimo lineages, occurring at least 4000 years ago. Rationale We addressed the genetic origins and relationships of the various New World Arctic cultures to each other and to modern-day populations in the region. We obtained 26 genome-wide sequences and 169 mitochondrial DNA sequences from ancient human bone, teeth, and hair samples from Arctic Siberia, Alaska, Canada, and Greenland, and high-coverage genomes of two present-day Greenlandic Inuit, two Siberian Nivkhs, one Aleutian Islander, and two Athabascan Native Americans. Twenty-seven ancient samples were radiocarbon dated for accurate cultural assignment, of which 25 were corrected for marine reservoir effect to account for the dominant marine component in these individuals’ diets. Results Nuclear and mitochondrial DNA data unequivocally show that the Paleo-Eskimos are closer to each other than to any other present-day population. The Thule culture represents a distinct people that are genetic and cultural ancestors of modern-day Inuit. We additionally find the Siberian Birnirk culture (6th to 7th century CE) as likely cultural and genetic ancestors of the Thule. The extinct Sadlermiut people from the Hudson Bay region (15th to 19th century CE), considered to be Dorset remnants, are genetically closely related to Thule/Inuit, rather than the Paleo-Eskimos. Moreover, there is no evidence of matrilineal gene flow between Dorset or Thule groups with neighboring Norse (Vikings) populations settling in the Arctic around 1000 years ago. However, we do detect gene flow between the Paleo-Eskimo and Neo-Eskimo lineages, dating back to at least 4000 years. Conclusion Our study has a number of important implications: Paleo-Eskimos likely represent a single migration pulse into the Americas from Siberia, separate from the ones giving rise to the Inuit and other Native Americans, including Athabascan speakers. Paleo-Eskimos, despite showing cultural differences across time and space, constituted a single population displaying genetic continuity for more than 4000 years. On the contrary, the Thule people, ancestors of contemporary Inuit, represent a population replacement of the Paleo-Eskimos that occurred less than 700 years ago. The long-term genetic continuity of the Paleo-Eskimo gene pool and lack of evidence of Native American admixture suggest that the Saqqaq and Dorset people were largely living in genetic isolation after entering the New World. Thus, the Paleo-Eskimo technological innovations and changes through time, as evident from the archaeological record, seem to have occurred solely by movement of ideas within a single resident population. This suggests that cultural similarities and differences are not solid proxies for population movements and migrations into new and dramatically different environments, as is often assumed. Arctic genetics comes in from the cold Despite a well-characterized archaeological record, the genetics of the people who inhabit the Arctic have been unexplored. Raghavan et al. sequenced ancient and modern genomes of individuals from the North American Arctic (see the Perspective by Park). Analyses of these genomes indicate that the Arctic was colonized 6000 years ago by a migration separate from the one that gave rise to other Native American populations. Furthermore, the original paleo-inhabitants of the Arctic appear to have been completely replaced approximately 700 years ago. Science, this issue 10.1126/science.1255832; see also p. 1004 Early Arctic humans differed from both present-day Inuit and Native Americans. [Also see Perspective by Park] The New World Arctic, the last region of the Americas to be populated by humans, has a relatively well-researched archaeology, but an understanding of its genetic history is lacking. We present genome-wide sequence data from ancient and present-day humans from Greenland, Arctic Canada, Alaska, Aleutian Islands, and Siberia. We show that Paleo-Eskimos (~3000 BCE to 1300 CE) represent a migration pulse into the Americas independent of both Native American and Inuit expansions. Furthermore, the genetic continuity characterizing the Paleo-Eskimo period was interrupted by the arrival of a new population, representing the ancestors of present-day Inuit, with evidence of past gene flow between these lineages. Despite periodic abandonment of major Arctic regions, a single Paleo-Eskimo metapopulation likely survived in near-isolation for more than 4000 years, only to vanish around 700 years ago.

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.

High frequency of lactose intolerance in a prehistoric hunter-gatherer population in northern Europe

BackgroundGenes and culture are believed to interact, but it has been difficult to find direct evidence for the process. One candidate example that has been put forward is lactase persistence in adulthood, i.e. the ability to continue digesting the milk sugar lactose after childhood, facilitating the consumption of raw milk. This genetic trait is believed to have evolved within a short time period and to be related with the emergence of sedentary agriculture.ResultsHere we investigate the frequency of an allele (-13910*T) associated with lactase persistence in a Neolithic Scandinavian population. From the 14 individuals originally examined, 10 yielded reliable results. We find that the T allele frequency was very low (5%) in this Middle Neolithic hunter-gatherer population, and that the frequency is dramatically different from the extant Swedish population (74%).ConclusionsWe conclude that this difference in frequency could not have arisen by genetic drift and is either due to selection or, more likely, replacement of hunter-gatherer populations by sedentary agriculturalists.

Establishing the validity of domestication genes using DNA from ancient chickens

Significance Recent studies have identified the genetic basis of numerous traits that differentiate modern domestic species from their wild counterparts. In both plants and animals, traits (and the genes underlying them) found ubiquitously in modern breeds are often presumed to have been selected early during the domestication process. Here, by determining genetic variability in ancient European chickens over the past 2,000 years, we show that a mutation thought to be crucial during chicken domestication was not subjected to strong human-mediated selection until much later in time. This result demonstrates that the ubiquity of mutations, which differentiate modern wild and domestic taxa, does not necessarily imply ancient origins. Modern domestic plants and animals are subject to human-driven selection for desired phenotypic traits and behavior. Large-scale genetic studies of modern domestic populations and their wild relatives have revealed not only the genetic mechanisms underlying specific phenotypic traits, but also allowed for the identification of candidate domestication genes. Our understanding of the importance of these genes during the initial stages of the domestication process traditionally rests on the assumption that robust inferences about the past can be made on the basis of modern genetic datasets. A growing body of evidence from ancient DNA studies, however, has revealed that ancient and even historic populations often bear little resemblance to their modern counterparts. Here, we test the temporal context of selection on specific genetic loci known to differentiate modern domestic chickens from their extant wild ancestors. We extracted DNA from 80 ancient chickens excavated from 12 European archaeological sites, dated from ∼280 B.C. to the 18th century A.D. We targeted three unlinked genetic loci: the mitochondrial control region, a gene associated with yellow skin color (β-carotene dioxygenase 2), and a putative domestication gene thought to be linked to photoperiod and reproduction (thyroid-stimulating hormone receptor, TSHR). Our results reveal significant variability in both nuclear genes, suggesting that the commonality of yellow skin in Western breeds and the near fixation of TSHR in all modern chickens took place only in the past 500 y. In addition, mitochondrial variation has increased as a result of recent admixture with exotic breeds. We conclude by emphasizing the perils of inferring the past from modern genetic data alone.

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.

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.

Barking up the wrong tree Modern northern European dogs fail to explain their origin

BackgroundGeographic distribution of the genetic diversity in domestic animals, particularly mitochondrial DNA, has often been used to infer centers of domestication. The underlying presumption is that phylogeographic patterns among domesticates were established during, or shortly after the domestication. Human activities are assumed not to have altered the haplogroup frequencies to any great extent. We studied this hypothesis by analyzing 24 mtDNA sequences in ancient Scandinavian dogs. Breeds originating in northern Europe are characterized by having a high frequency of mtDNA sequences belonging to a haplogroup rare in other populations (HgD). This has been suggested to indicate a possible origin of the haplogroup (perhaps even a separate domestication) in central or northern Europe.ResultsThe sequences observed in the ancient samples do not include the haplogroup indicative for northern European breeds (HgD). Instead, several of them correspond to haplogroups that are uncommon in the region today and that are supposed to have Asian origin.ConclusionWe find no evidence for local domestication. We conclude that interpretation of the processes responsible for current domestic haplogroup frequencies should be carried out with caution if based only on contemporary data. They do not only tell their own story, but also that of humans.