The population dynamics that followed the Out of Africa (OoA) expansion and the whereabouts of the early migrants before the differentiation that ultimately led to the formation of Oceanian, West and East Eurasian macropopulations have long been debated. Shedding light on these events may, in turn, provide clues to better understand the cultural evolution in Eurasia between 50 and 35 ka. Here, we analyze Eurasian Paleolithic DNA evidence to provide a comprehensive population model and validate it in light of available material culture. Leveraging on our integrated approach we propose the existence of a Eurasian population Hub, where Homo sapiens lived between the OoA and the broader colonization of Eurasia, which was characterized by multiple events of expansion and local extinction. A major population wave out of Hub, of which Ust’Ishim, Bacho Kiro, and Tianyuan are unadmixed representatives, is broadly associated with Initial Upper Paleolithic lithics and populated West and East Eurasia before or around 45 ka, before getting largely extinct in Europe. In this light, we suggest a parsimonious placement of Oase1 as an individual related to Bacho Kiro who experienced additional Neanderthal introgression. Another expansion, started before 38 ka, is broadly associated with Upper Paleolithic industries and repopulated Europe with sporadic admixtures with the previous wave (GoyetQ116-1) and more systematic ones, whereas moving through Siberia (Yana, Mal’ta). Before these events, we also confirm Zlatý Kůň as the most basal human lineage sequenced to date OoA, potentially representing an earlier wave of expansion out of the Hub.

Highlights d Ancient groups differentially contributed to complex traits in contemporary Europeans d In contemporary Estonians 11 out of 27 traits show association with some ancestry d Hunter-Gatherer and Yamnaya ancestries divergently influence cholesterol levels d Post-admixture selection is not necessary to have traitancestry associations

The contemporary European genetic makeup formed in the last 8000 years as the combination of three main genetic components: the local Western Hunter-Gatherers, the incoming Neolithic Farmers from Anatolia and the Bronze Age component from the Pontic Steppes. When meeting into the post-Neolithic European environment, the genetic variants accumulated during their three distinct evolutionary histories mixed and came into contact with new environmental challenges. Here we investigate how this genetic legacy reflects on the complex trait landscape of contemporary European populations, using the Estonian Biobank as a case study. For the first time we directly connect the phenotypic information available from biobank samples with the genetic similarity to these ancestral groups, both at a genome-wide level and focusing on genomic regions associated with each of the 27 complex traits we investigated. We also found SNPs connected to pigmentation, cholesterol, sleep, diastolic blood pressure, and body mass index (BMI) to show signals of selection following the post Neolithic admixture events. We recapitulate existing knowledge about pigmentation traits, corroborate the connection between Steppe ancestry and height and highlight novel associations. Among others, we report the contribution of Hunter Gatherer ancestry towards high BMI and low blood cholesterol levels. Our results show that the ancient components that form the contemporary European genome were differentiated enough to contribute ancestry-specific signatures to the phenotypic variability displayed by contemporary individuals in at least 11 out of 27 of the complex traits investigated here.

The population dynamics that followed the out of Africa expansion (OoA) and ultimately led to the formation of Oceanian, West and East Eurasian macro populations have long been debated. Furthermore, with the OoA being dated between 70 kya and 65 kya and the earliest splits between West and East Eurasian populations being inferred not earlier than 43 kya from modern DNA data, an additional question concerns the whereabouts of the early migrants out of Africa before those differentiations. Shedding light on these population dynamics may, in turn, provide clues to better understand cultural evolution in Eurasia between 50 kya and 35 kya, where the development of new technologies may be correlated to parallel independent evolution paths, to the arrival of new populations, or to long-term processes of cultural and biological exchanges. Here we jointly re-analyze Eurasian Paleolithic DNA available to date in light of material culture, and provide a comprehensive population model with minimal admixture events. Our integrated approach i) maintains Zlaty Kůň genetically as the most basal out of Africa human lineage sequenced to date, also in comparison to Oceanians and putatively links it with non-Mousterian material cultures documented in Europe 48-43 kya; ii) infers the presence of an OoA population Hub from which a major wave broadly associated with Initial Upper Paleolithic lithic industries emanated to populate West and East Eurasia before or around 45 kya, and of which Ust′Ishim, Bacho Kiro and Tianyuan were unadmixed descendants; iii) proposes a parsimonious placement of Oase1 as an individual related to Bacho Kiro who experienced additional Neanderthal introgression; and iv) explains the East/West Eurasian population split as a longer permanence of the latter in the OoA Hub, followed by a second population expansion (before 37 kya), broadly associated with Upper Paleolithic industries, that largely replaced pre-existing humans in Europe, and admixed with the previous wave to form Yana and Mal′ta in Siberia and, to a greater extent, GoyetQ116-1 in Belgium.

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