To learn more about humans of the past, we extract DNA from archaeological skeletons and sequence their genomes. Then we use biostatistic and population genetic approaches to infer their evolutionary and demographic history.
Our understanding of prehistoric societal organization at the family level is still limited. Here, we generated genome data from 32 individuals from an approximately 3,800-y-old
burial mound attributed to the Bronze Age Srubnaya-Alakul cultural tradition at the site of Nepluyevsky, located in the Southern Ural region of Central Eurasia. We found that life expectancy was generally very low, with adult males living on average 8 y longer than females. A total of 35 first-degree, 40 second-degree, and 48 third-degree biological relationships connected 23 of the studied individuals, allowing us to propose a family tree spanning three generations with six brothers at its center. The oldest of these brothers had eight children with two women and the most children overall, whereas the other relationships were monogamous. Notably, related female children above the age of five
were completely absent from the site, and adult females were more genetically diverse than males. These results suggest that biological relationships between male siblings
played a structural role in society and that descent group membership was based on patrilineality. Women originated from a larger mating network and moved to join the
men, with whom they were buried. Finally, the oldest brother likely held a higher social position, which was expressed in terms of fertility.
Jens Blöcher, Maxime Brami, Isabelle Sofie Feinauer, Eliza Stolarczyk, Yoan Diekmann, Lisa Vetterdietz, Marina Karapetian, Laura Winkelbach, Vanessa Kokot, Leonardo Vallini, Astrid Strobbe, Wolfgang Haak, Christina Papageorgopoulou, Rüdiger Krause, Svetlana Sharapova, Joachim Burger (2023)
Genomic regions under positive selection harbor variation linked for example to adaptation. Most tools for detecting positively selected variants have computational resource requirements rendering them impractical on population genomic datasets with hundreds of thousands of individuals or more. We have developed and implemented an efficient haplotype-based approach able to scan large datasets and accurately detect positive selection. We achieve this by combining a pattern matching approach based on the positional Burrows–Wheeler transform with model-based inference which only requires the evaluation of closed-form expressions. We evaluate our approach with simulations,
and find it to be both sensitive and specific. The computational resource requirements quantified using UK Biobank data indicate that our implementation is scalable to population genomic datasets with millions of individuals. Our approach may serve as an algorithmic blueprint for the era of “big data” genomics: a combinatorial core coupled with statistical inference in closed form.
Benedikt Kirsch-Gerweck, Leonard Bohnenkämper, Michel T. Henrichs, Jarno N. Alanko, Hideo Bannai, Bastien Cazaux, Pierre Peterlongo, Joachim Burger, Jens Stoye and Yoan Diekmann (2023)
It is now widely accepted that agriculture and settled village life arrived in Europe as a cultural package, carried by people migrating from Anatolia and the Aegean Basin. The putative fisher-forager site of Lepenski Vir in Serbia has long been acknowledged as an exception to this model. Here, the Mesolithic–Neolithic transition—possibly inspired by interaction with the new arrivals—was thought to have taken place autochthonously on site. Our reinterpretation, based on ancient genomes, as well as archaeological and isotopic evidence, indicates that here, too, house construction, early village society and agriculture were primarily associated with Europe’s first farmers, thus challenging the long-held view of Lepenski Vir as a Mesolithic community that adopted Neolithic practices. Although aspects of the site’s occupation, such as the trapezoidal houses, were inspired by local Mesolithic traditions, it is far from certain that the village was founded by Iron Gates foragers. A detailed timeline of population changes at the site suggests that Aegean incomers did not simply integrate into an established Mesolithic society, but rather founded new lineages and households. Iron Gates foragers and their admixed descendants largely appear to have been buried separately, on the fringes of the settlement. The diet of those buried outside in pits shows no major shift from aquatic to terrestrial food resources.
Maxime Brami, Laura Winkelbach, Ilektra Schulz, Mona Schreiber, Jens Blöcher, Yoan Diekmann, and Joachim Burger (2022)
The precise genetic origins of the first Neolithic farming populations in Europe and Southwest Asia, as well as the processes and the timing of their differentiation, remain largely unknown. Demogenomic modeling of high-quality ancient genomes reveals that the early farmers of Anatolia and Europe emerged from a multiphase mixing of a Southwest Asian population with a strongly bottlenecked western hunter-gatherer population after the last glacial maximum. Moreover, the ancestors of the first farmers of Europe and Anatolia went through a period of extreme genetic drift during their westward range expansion, contributing highly to their genetic distinctiveness. This modeling elucidates the demographic processes at the root of the Neolithic transition and leads to a spatial interpretation of the population history of Southwest Asia and Europe during the late Pleistocene and early Holocene.
Nina Marchi, Laura Winkelbach, Ilektra Schulz, Maxime Brami, Zuzana Hofmanová, Jens Blöcher, Carlos S. Reyna-Blanco, Yoan Diekmann, Alexandre Thiéry, Adamandia Kapopoulou, Vivian Link, Valérie Piuz, Susanne Kreutzer, Sylwia M. Figarska, Elissavet Ganiatsou, Albert Pukaj, Travis J. Struck, Ryan N. Gutenkunst, Necmi Karul, Fokke Gerritsen, Joachim Pechtl, Joris Peters, Andrea Zeeb-Lanz, Eva Lenneis, Maria Teschler-Nicola, Sevasti Triantaphyllou, Sofija Stefanovic, Christina Papageorgopoulou, Daniel Wegmann, Joachim Burger, and Laurent Excoffier (2022)
Lactase persistence (LP), the continued expression of lactase into adulthood, is the most strongly selected single gene trait over the last 10,000 years in multiple human populations. It has been posited that the primary allele causing LP among Eurasians, rs4988235-A , only rose to appreciable frequencies during the Bronze and Iron Ages [2, 3], long after humans started consuming milk from domesticated animals. This rapid rise has been attributed to an influx of people from the Pontic-Caspian steppe that began around 5,000 years ago [4, 5]. We investigate the spatiotemporal spread of LP through an analysis of 14 warriors from the Tollense Bronze Age battlefield in northern Germany (∼3,200 before present, BP), the oldest large-scale conflict site north of the Alps. Genetic data indicate that these individuals represent a single unstructured Central/Northern European population. We complemented these data with genotypes of 18 individuals from the Bronze Age site Mokrin in Serbia (∼4,100 to ∼3,700 BP) and 37 individuals from Eastern Europe and the Pontic-Caspian Steppe region, predating both Bronze Age sites (∼5,980 to ∼3,980 BP). We infer low LP in all three regions, i.e., in northern Germany and South-eastern and Eastern Europe, suggesting that the surge of rs4988235 in Central and Northern Europe was unlikely caused by Steppe expansions. We estimate a selection coefficient of 0.06 and conclude that the selection was ongoing in various parts of Europe over the last 3,000 years.
Joachim Burger, Vivian Link, Jens Blöcher, Anna Schulz, Christian Sell, Zoé Pochon, Yoan Diekmann, Aleksandra Žegarac, Zuzana Hofmanová, Laura Winkelbach, Carlos S. Reyna-Blanco, Vanessa Bieker, Jörg Orschiedt, Ute Brinker, Amelie Scheu, Christoph Leuenberger, Thomas S. Bertino, Ruth Bollongino, Gundula Lidke, Sofija Stefanović, Detlef Jantzen, Elke Kaiser, Thomas Terberger, Mark G. Thomas, Krishna R. Veeramah and Daniel Wegmann (2020)
Modern European genetic structure demonstrates strong correlations with geography, while genetic analysis of prehistoric humans has indicated at least two major waves of immigration from outside the continent during periods of cultural change. However, population-level genome data that could shed light on the demographic processes occurring during the intervening periods have been absent. Therefore, we generated genomic data from 41 individuals dating mostly to the late 5th/early 6th century AD from present-day Bavaria in southern Germany, including 11 whole genomes (mean depth 5.56×). In addition we developed a capture array to sequence neutral regions spanning a total of 5 Mb and 486 functional polymorphic sites to high depth (mean 72×) in all individuals. Our data indicate that while men generally had ancestry that closely resembles modern northern and central Europeans, women exhibit a very high genetic heterogeneity; this includes signals of genetic ancestry ranging from western Europe to East Asia. Particularly striking are women with artificial skull deformations; the analysis of their collective genetic ancestry suggests an origin in southeastern Europe. In addition, functional variants indicate that they also differed in visible characteristics. This example of female-biased migration indicates that complex demographic processes during the Early Medieval period may have contributed in an unexpected way to shape the modern European genetic landscape. Examination of the panel of functional loci also revealed that many alleles associated with recent positive selection were already at modern-like frequencies in European populations ∼1,500 years ago.
Krishna R. Veeramah, Andreas Rott, Melanie Groß, Lucy van Dorp, Saioa López, Karola Kirsanow, Christian Sell, Jens Blöcher, Daniel Wegmann, Vivian Link, Zuzana Hofmanová, Joris Peters, Bernd Trautmann, Anja Gairhos, Jochen Haberstroh, Bernd Päffgen, Garrett Hellenthal, Brigitte Haas-Gebhard, Michaela Harbeck and Joachim Burger (2018)
We sequenced Early Neolithic genomes from the Zagros region of Iran (eastern Fertile Crescent), where some of the earliest evidence for farming is found, and identify a previously uncharacterized population that is neither ancestral to the first European farmers nor has contributed significantly to the ancestry of modern Europeans. These people are estimated to have separated from Early Neolithic farmers in Anatolia some 46-77,000 years ago and show affinities to modern day Pakistani and Afghan populations, but particularly to Iranian Zoroastrians. We conclude that multiple, genetically differentiated hunter-gatherer populations adopted farming in SW-Asia, that components of pre-Neolithic population structure were preserved as farming spread into neighboring regions, and that the Zagros region was the cradle of eastward expansion.
Farnaz Broushaki, Mark G. Thomas, Vivian Link, Saioa López, Lucy van Dorp, Karola Kirsanow, Zuzana Hofmanová, Yoan Diekmann, Lara M. Cassidy, David Díez-del-Molino, Athanasios Kousathanas, Christian Sell, Harry K. Robson, Rui Martiniano, Jens Blöcher, Amelie Scheu, Susanne Kreutzer, Ruth Bollongino, Dean Bobo, Hossein Davudi, Olivia Munoz, Mathias Currat, Kamyar Abdi, Fereidoun Biglari, Oliver E. Craig, Daniel G. Bradley, Stephen Shennan, Krishna Veeramah, Marjan Mashkour, Daniel Wegmann, Garrett Hellenthal, Joachim Burger (2016)
Farming and sedentism first appear in southwest Asia during the early Holocene and later spread to neighboring regions, including Europe, along multiple dispersal routes. Conspicuous uncertainties remain about the relative roles of migration, cultural diffusion and admixture with local foragers in the early Neolithisation of Europe. Here we present paleogenomic data for five Neolithic individuals from northern Greece and northwestern Turkey – spanning the time and region of the earliest spread of farming into Europe. We observe striking genetic similarity both among Aegean early farmers and with those from across Europe. Our study demonstrates a direct genetic link between Mediterranean and Central European early farmers and those of Greece and Anatolia, extending the European Neolithic migratory chain all the way back to southwestern Asia.
Zuzana Hofmanová, Susanne Kreutzer, Garrett Hellenthal, Christian Sell, Yoan Diekmann, David Díez-del-Molino, Lucy van Dorp, Saioa López, Athanasios Kousathanas, Vivian Link, Karola Kirsanow, Lara M. Cassidy, Rui Martiniano, Melanie Strobel, Amelie Scheu, Kostas Kotsakis, Paul Halstead, Sevi Triantaphyllou, Nina Kyparissi-Apostolika, Dushanka-Christina Urem-Kotsou, Christina Ziota, Fotini Adaktylou, Shyamalika Gopalan, Dean M. Bobo, Laura Winkelbach, Jens Blöcher, Martina Unterländer, Christoph Leuenberger, Çiler Çilingiroğlu, Barbara Horejs, Fokke Gerritsen, Stephen Shennan, Daniel G. Bradley, Mathias Currat, Krishna R. Veeramah, Daniel Wegmann, Mark G. Thomas, Christina Papageorgopoulou, and Joachim Burger (2016)
We sequenced the genomes of an approximately 7,000-year-old farmer from Germany and eight approximately 8,000-year-old hunter-gatherers from Luxembourg and Sweden. We analysed these and other ancient genomes with 2,345 contemporary humans to show that most present-day Europeans derive from at least three highly differentiated populations: west European hunter-gatherers, who contributed ancestry to all Europeans but not to Near Easterners; ancient north Eurasians related to Upper Palaeolithic Siberians, who contributed to both Europeans and Near Easterners; and early European farmers, who were mainly of Near Eastern origin but also harboured west European hunter-gatherer related ancestry. We model these populations’ deep relationships and show that early European farmers had approximately 44% ancestry from a ‘basal Eurasian’ population that split before the diversification of other non-African lineages.
Iosif Lazaridis, Nick Patterson, Alissa Mittnik, Gabriel Renaud, Swapan Mallick, Karola Kirsanow, Peter H. Sudmant, Joshua G. Schraiber, Sergi Castellano, Mark Lipson, Bonnie Berger, Christos Economou, Ruth Bollongino, Qiaomei Fu, Kirsten I. Bos, Susanne Nordenfelt, Heng Li, Cesare de Filippo, Kay Prüfer, Susanna Sawyer, Cosimo Posth, Wolfgang Haak, Fredrik Hallgren, Elin Fornander, Nadin Rohland, Dominique Delsate, Michael Francken, Jean-Michel Guinet, Joachim Wahl, George Ayodo, Hamza A. Babiker, Graciela Bailliet, Elena Balanovska, Oleg Balanovsky, Ramiro Barrantes, Gabriel Bedoya, Haim Ben-Ami, Judit Bene, Fouad Berrada, Claudio M. Bravi, Francesca Brisighelli, George B. J. Busby, Francesco Cali, Mikhail Churnosov, David E. C. Cole, Daniel Corach, Larissa Damba, George van Driem, Stanislav Dryomov, Jean-Michel Dugoujon, Sardana A. Fedorova, Irene Gallego Romero, Marina Gubina, Michael Hammer, Brenna M. Henn, Tor Hervig, Ugur Hodoglugil, Aashish R. Jha, Sena Karachanak-Yankova, Rita Khusainova, Elza Khusnutdinova, Rick Kittles, Toomas Kivisild, William Klitz, Vaidutis Kučinskas, Alena Kushniarevich, Leila Laredj, Sergey Litvinov, Theologos Loukidis, Robert W. Mahley, Be’la Melegh, Ene Metspalu, Julio Molina, Joanna Mountain, Klemetti Nakkalajarvi, Desislava Nesheva, Thomas Nyambo, Ludmila Osipova, Juri Parik, Fedor Platonov, Olga Posukh, Valentino Romano, Francisco Rothhammer, Igor Rudan, Ruslan Ruizbakiev, Hovhannes Sahakyan, Antti Sajantila, Antonio Salas, Elena B. Starikovskaya, Ayele Tarekegn, Draga Toncheva, Shahlo Turdikulova, Ingrida Uktveryte, Olga Utevska, René Vasquez, Mercedes Villena, Mikhail Voevoda, Cheryl A. Winkler, Levon Yepiskoposyan, Pierre Zalloua, Tatijana Zemunik, Alan Cooper, Cristian Capelli, Mark G.Thomas, Andres Ruiz-Linares, Sarah A. Tishkoff, Lalji Singh, Kumarasamy Thangaraj, Richard Villems, David Comas, Rem Sukernik, Mait Metspalu, Matthias Meyer, Evan E. Eichler, Joachim Burger, Montgomery Slatkin, Svante Pääbo, Janet Kelso, David Reich, Johannes Krause (2014)
Pigmentation is a polygenic trait encompassing some of the most visible phenotypic variation observed in humans. Here we present direct estimates of selection acting on functional alleles in three key genes known to be involved in human pigmentation pathways – HERC2, SLC45A2, and TYR – using allele frequency estimates from Eneolithic, Bronze Age, and modern Eastern European samples and forward simulations. Neutrality was overwhelmingly rejected for all alleles studied, with point estimates of selection ranging from around 2–10% per generation. Our results provide direct evidence that strong selection favoring lighter skin, hair, and eye pigmentation has been operating in European populations over the last 5,000 y.
Sandra Wilde, Adrian Timpson, Karola Kirsanow, Elke Kaiser, Manfred Kayser, Martina Unterländer, Nina Hollfelder, Inna D. Potekhina, Wolfram Schier, Mark G. Thomas, and Joachim Burger (2014)
Debate on the ancestry of Europeans centers on the interplay between Mesolithic foragers and Neolithic farmers. Foragers are generally believed to have disappeared shortly after the arrival of agriculture. To investigate the relation between foragers and farmers, we examined Mesolithic and Neolithic samples from the Blätterhohle site. Mesolithic mitochondrial DNA sequences were typical of European foragers, whereas the Neolithic sample included additional lineages that are associated with early farmers. However, isotope analyses separate the Neolithic sample into two groups: one with an agriculturalist diet and one with a forager and freshwater fish diet, the latter carrying mitochondrial DNA sequences typical of Mesolithic hunter-gatherers. This indicates that the descendants of Mesolithic people maintained a foraging lifestyle in Central Europe for more than 2000 years after the arrival of farming societies.
Ruth Bollongino, Olaf Nehlich, Michael P. Richards, Jörg Orschiedt, Mark G. Thomas, Christian Sell, Zuzana Fajkošová, Adam Powell, Joachim Burger (2013)
Lactase persistence, the ability to digest the milk sugar lactose in adulthood, is highly associated with a T allele situated 13,910 bp upstream from the actual lactase gene in Europeans. The frequency of this allele rose rapidly in Europe after transition from hunter-gatherer to agriculturalist lifestyles and the introduction of milkable domestic species from Anatolia some 8000 years ago. Here we first introduce the archaeological and historic background of early farming life in Europe, then summarize what is known of the physiological and genetic mechanisms of lactase persistence. Finally, we compile the evidence for a co-evolutionary process between dairying culture and lactase persistence. We describe the different hypotheses on how this allele spread over Europe and the main evolutionary forces shaping this process. We also summarize three different computer simulation approaches, which offer a means of developing a coherent and integrated understanding of the process of spread of lactase persistence and dairying.
Michela Leonardi, Pascale Gerbault, Mark G. Thomas, Joachim Burger (2012)
After the domestication of animals and crops in the Near East some 11,000 years ago, farming had reached much of central Europe by 7500 years before the present. The extent to which these early European farmers were immigrants or descendants of resident hunter-gatherers who had adopted farming has been widely debated. We compared new mitochondrial DNA (mtDNA) sequences from late European hunter-gatherer skeletons with those from early farmers and from modern Europeans. We find large genetic differences between all three groups that cannot be explained by population continuity alone. Most (82%) of the ancient hunter-gatherers share mtDNA types that are relatively rare in central Europeans today. Together, these analyses provide persuasive evidence that the first farmers were not the descendants of local hunter-gatherers but immigrated into central Europe at the onset of the Neolithic.
Barbara Bramanti, Mark. G. Thomas, Wolfgang Haak, Martina Unterländer, Pia C. Jores, Kristiina Tambets, I.Antanaitis-Jacobs, Miriam N. Haidle, Rimantas Jankauskas, C.-J. Kind, Friedrich Lueth, Thomas Terberger, J. Hiller, S. Matsumura, P. Forster, Joachim Burger (2009)
Lactase persistence (LP) is common among people of European ancestry, but with the exception of some African, Middle Eastern and southern Asian groups, is rare or absent elsewhere in the world. Lactase gene haplotype conservation around a polymorphism strongly associated with LP in Europeans (–13,910 C/T) indicates that the derived allele is recent in origin and has been subject to strong positive selection. Furthermore, ancient DNA work has shown that the –13,910*T (derived) allele was very rare or absent in early Neolithic central Europeans. It is unlikely that LP would provide a selective advantage without a supply of fresh milk, and this has lead to a gene-culture coevolutionary model where lactase persistence is only favoured in cultures practicing dairying, and dairying is more favoured in lactase persistent populations. We have developed a flexible demic computer simulation model to explore the spread of lactase persistence, dairying, other subsistence practices and unlinked genetic markers in Europe and western Asia’s geographic space. Using data on –13,910*T allele frequency and farming arrival dates across Europe, and approximate Bayesian computation to estimate parameters of interest, we infer that the –13,910*T allele first underwent selection among dairying farmers around 7,500 years ago in a region between the central Balkans and central Europe, possibly in association with the dissemination of the Neolithic Linearbandkeramik culture over Central Europe. Furthermore, our results suggest that natural selection favouring a lactase persistence allele was not higher in northern latitudes through an increased requirement for dietary vitamin D. Our results provide a coherent and spatially explicit picture of the coevolution of lactase persistence and dairying in Europe.
Yuval Itan, Adam Powell, Mark A. Beaumont, Joachim Burger, Mark G. Thomas (2009)
Lactase persistence (LP), the dominant Mendelian trait conferring the ability to digest the milk sugar lactose in adults, has risen to high frequency in central and northern Europeans in the last 20,000 years. This trait is likely to have conferred a selective advantage in individuals who consume appreciable amounts of unfermented milk. Some have argued for the “culture-historical hypothesis,” whereby LP alleles were rare until the advent of dairying early in the Neolithic but then rose rapidly in frequency under natural selection. Others favor the “reverse cause hypothesis,” whereby dairying was adopted in populations with preadaptive high LP allele frequencies. Analysis based on the conservation of lactase gene haplotypes indicates a recent origin and high selection coefficients for LP, although it has not been possible to say whether early Neolithic European populations were lactase persistent at appreciable frequencies. We developed a stepwise strategy for obtaining reliable nuclear ancient DNA from ancient skeletons, based on (i) the selection of skeletons from archaeological sites that showed excellent biomolecular preservation, (ii) obtaining highly reproducible human mitochondrial DNA sequences, and (iii) reliable short tandem repeat (STR) genotypes from the same specimens. By applying this experimental strategy, we have obtained high-confidence LP-associated genotypes from eight Neolithic and one Mesolithic human remains, using a range of strict criteria for ancient DNA work. We did not observe the allele most commonly associated with LP in Europeans, thus providing evidence for the culture-historical hypothesis, and indicating that LP was rare in early European farmers.
Joachim Burger, Martina Kirchner, Barbara Bramanti, Wolfgang Haak, Mark G. Thomas (2007)
The ancestry of modern Europeans is a subject of debate among geneticists, archaeologists, and anthropologists. A crucial question is the extent to which Europeans are descended from the first European farmers in the Neolithic Age 7500 years ago or from Paleolithic hunter-gatherers who were present in Europe since 40,000 years ago. Here we present an analysis of ancient DNA from early European farmers. We successfully extracted and sequenced intact stretches of maternally inherited mitochondrial DNA (mtDNA) from 24 out of 57 Neolithic skeletons from various locations in Germany, Austria, and Hungary. We found that 25% of the Neolithic farmers had one characteristic mtDNA type and that this type formerly was widespread among Neolithic farmers in Central Europe. Europeans today have a 150-times lower frequency (0.2%) of this mtDNA type, revealing that these first Neolithic farmers did not have a strong genetic influence on modern European female lineages. Our finding lends weight to a proposed Paleolithic ancestry for modern Europeans.
Wolfgang Haak, Peter Forster, Barbara Bramanti, Shuichi Matsumura, Guido Brandt, Marc Tänzer, Richard Villems, Colin Renfrew, Detlef Gronenborn, Kurt W. Alt, Joachim Burger (2005)