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Genomic ancestry, diet and microbiomes of Upper Palaeolithic hunter-gatherers from San Teodoro cave
Abstract
Recent improvements in the analysis of ancient biomolecules from human remains and associated dental calculus have provided new insights into the prehistoric diet and genetic diversity of our species. Here we present a multi-omics study, integrating metagenomic and proteomic analyses of dental calculus, and human ancient DNA analysis of the petrous bones of two post-Last Glacial Maximum (LGM) individuals from San Teodoro cave (Italy), to reconstruct their lifestyle and the post-LGM resettlement of Europe. Our analyses show genetic homogeneity in Sicily during the Palaeolithic, representing a hitherto unknown Italian genetic lineage within the previously identified Villabruna cluster. We argue that this lineage took refuge in Italy during the LGM, followed by a subsequent spread to central-western Europe. Analysis of dental calculus showed a diet rich in animal proteins which is also reflected on the oral microbiome composition. Our results demonstrate the power of this approach in the study of prehistoric humans and will enable future research to reach a more holistic understanding of the population dynamics and ecology.
https://www.nature.com/articles/s42003-022-04190-2
Abstract
Recent improvements in the analysis of ancient biomolecules from human remains and associated dental calculus have provided new insights into the prehistoric diet and genetic diversity of our species. Here we present a multi-omics study, integrating metagenomic and proteomic analyses of dental calculus, and human ancient DNA analysis of the petrous bones of two post-Last Glacial Maximum (LGM) individuals from San Teodoro cave (Italy), to reconstruct their lifestyle and the post-LGM resettlement of Europe. Our analyses show genetic homogeneity in Sicily during the Palaeolithic, representing a hitherto unknown Italian genetic lineage within the previously identified Villabruna cluster. We argue that this lineage took refuge in Italy during the LGM, followed by a subsequent spread to central-western Europe. Analysis of dental calculus showed a diet rich in animal proteins which is also reflected on the oral microbiome composition. Our results demonstrate the power of this approach in the study of prehistoric humans and will enable future research to reach a more holistic understanding of the population dynamics and ecology.
Genetic structure of European Hunter-Gatherers
For the purpose of analysing the genetic diversity of European hunter-gatherers after the LGM, we merged the data from San Teodoro with a panel of previously published hunter-gatherer individuals (Palaeolithic and Mesolithic) from across Europe (Fig. 1a). To visualise the genetic structure of the ancient individuals, we performed multidimensional scaling on a distance matrix derived from pairwise identity-by-state (IBS) sharing of alleles among individuals (Fig. 1b, Supplementary Fig. 9). The two San Teodoro samples fell broadly within the genetic diversity of individuals from western and southern Europe, previously termed Western hunter-gatherers (WHG)19 (Fig. 1b, Supplementary Figs. 9–10). Within this group of individuals, San Teodoro clustered most closely with another Late Epigravettian individual from Sicily, Oriente C, and with the Late Upper Palaeolithic/Mesolithic individuals from Grotta Continenza (central Italy), indicating a common gene pool for post-LGM hunter-gatherers from the Italian peninsula from ~14,000 years ago onwards.
The clustering results are also confirmed by f4-statistics of the form f4(Mbuti, Test; SanTeodoro_LP.SG, DevilsCave_N.SG), which measures the excess of genetic drift a test individual shares with San Teodoro (from here on merged into a single population due to their high genetic similarity) compared to an outgroup (East Asian hunter-gatherers from Devil’s Gate cave). Results showed that WHG individuals, in particular those from the Italian peninsula, shared the highest amounts of genetic drift with San Teodoro. The highest affinity was observed for Oriente C (SIC2), an individual related to the same cultural sphere of San Teodoro (Late Epigravettian), with a similar age from the same geographic region (Sicily)20 (Fig. 1c, Supplementary Data 9).
Using f4-statistics of the form f4(Mbuti, Test; HG Italy, San_Teodoro_LP.SG), we next tested whether San Teodoro forms a clade with Italian hunter-gatherer groups, consisting of both Late Upper Palaeolithic (Oriente C, and Villabruna) and Late Upper Palaeolithic/Mesolithic (Continenza), to the exclusion of other test groups. While a clade-like relationship cannot be rejected for the Sicilian hunter-gatherer from Oriente C, significant statistics were observed in tests with the other two groups (Supplementary Fig. 11, Supplementary Data 10). For the central Italian individuals from Continenza, most post-LGM individuals showed significantly increased shared genetic drift compared to San Teodoro. The consistent magnitude of the statistics across individuals with a wide geographic distribution, and chrono-cultural differentiation, suggests possible gene flow between the ancestors of most post-LGM Europeans and Continenza, after their divergence from San Teodoro. Interestingly, the only individual with evidence for higher affinity with San Teodoro than with Continenza was the ~33,000-year-old pre-LGM individual Paglicci133 from Apulia in southern Italy (f4(Mbuti, Paglicci133; Italy_M.SG, San_Teodoro_LP.SG) = 0.003, Z = 2.6; Supplementary Figs. 9, 11). Paglicci 133 refers to Gravettian which is considered the cultural root (the Gravettian) from which the San Teodoro one (the Epigravettian) was derived in the following several millennia. This suggests possible gene flow involving ancestry related to pre-LGM hunter-gatherers in southern Italy, as previously observed on the Iberian Peninsula19, as a possible alternative explanation. A clade-like relationship was also rejected for the relationship of San Teodoro and the ~14,000-year-old northern Italian individual from Villabruna. In contrast to the results obtained with Continenza, in this analysis the individuals from western Europe mostly shared more genetic drift with San Teodoro, whereas individuals from eastern Europe shared more genetic drift with Villabruna (Supplementary Fig. 11, Supplementary Data 10). These results were also reflected in the genetic clustering, where Villabruna was shifted away from the Italian and west European individuals on a cline towards individuals from the Balkans (Iron Gates, Fig. 1b), suggesting further substructure among individuals of the Villabruna cluster.
The genetic diversity of European post-LGM hunter-gatherers has previously been described in terms of a west-to-east cline anchored by two major ancestry groups of western hunter-gatherers (WHG) and eastern hunter-gatherers (EHG)16, with some contributions from late Pleistocene hunter-gatherer ancestry in the Iberian Peninsula21. In the MDS in Fig. 1b, individuals were maximally differentiated in four distinct ancestry clusters, namely: (i) hunter-gatherers from the Italian peninsula (including San Teodoro), (ii) late Pleistocene hunter-gatherer ancestry (represented by Goyet Q-2), (iii) individuals from the Balkans (Iron Gates) and (iv) EHG from Russia. The remaining individuals were aligned across a number of distinct genetic clines, broadly related to their geographical location, including (Fig. 1b): (i) an Adriatic cline, linking the Italian peninsula to the Balkans; (ii) an Iberia late Pleistocene HG cline of Goyet Q-2 related ancestry in individuals from the Iberian peninsula; (iii) a Balkans-Ukraine cline and (iv) a NE Europe—Scandinavia—Russia cline, linking individuals from the Baltic to Scandinavia and EHG. Furthermore, we found evidence for temporal genetic structure within geographic regions. This was most notably at Iron Gates, where the earlier individuals from Serbia (before 9000 BP), together with the neighbouring individuals from Romania, form one of the four most differentiated clusters (Fig. 1b), whereas later individuals from Serbia (after 9000 BP) were shifted towards those from north-eastern Europe and the Baltics (Fig. 1b, Supplementary Fig. 12).
Motivated by these observations, we used qpAdm to infer ancestry proportions of European hunter-gatherers in a four-way model using representatives of the maximally differentiated genetic clusters as sources. The results recapitulated many of the features observed in the genetic clustering. In individuals from western Europe, ancestry related to Italian hunter-gatherers predominated, with varying contributions of late Pleistocene hunter-gatherer (Goyet Q-2) ancestry (Fig. 2, Supplementary Fig. 13, Supplementary Data 11–14). Late Pleistocene ancestry peaked in the Iberian Peninsula, with inferred ancestry proportions as high as 71% (El Miron), consistent with previous results21. An apparent influx of Balkan hunter-gatherer related ancestry was observed in the two most recent individuals from northern Iberia (La Brana, Los Canes), suggesting gene flow between distinct ancestry groups towards the end of the hunter-gatherer dominion in western Europe22. In eastern Europe, ancestry related to Balkan hunter-gatherers was most abundant, with additional contributions of Italian or EHG ancestry, in line with the geographic origin of the individuals. Genetic continuity could be rejected for many of the later Balkan hunter-gatherers from Iron Gates, which showed evidence for admixture with groups harbouring both Italian- and Goyet Q-2-related ancestry (Supplementary Fig. 13; Supplementary Data 11–14). Finally, EHG-related ancestry was found at highest proportions in individuals from Ukraine, as well as Scandinavian hunter-gatherers23. Once again, we observed temporal stratification in ancestry suggestive of local genetic transformations, with an increase in Balkan hunter-gatherer related ancestry in Ukrainian individuals after 10,000 BP16 (Supplementary Fig. 13). Taken together, these results document previously underappreciated complexity in the fine-scale genetic structure of post-LGM hunter-gatherers in Europe......
https://www.nature.com/articles/s42003-022-04190-2