doi: 10.1038/s41559-022-01952-3. Epub 2023 Jan 16.
Ancient DNA reveals admixture history and endogamy in the prehistoric Aegean
Eirini Skourtanioti 1 2 3, Harald Ringbauer 4 5 6, Guido Alberto Gnecchi Ruscone 4 5 7, Raffaela Angelina Bianco 5 7, Marta Burri 5 7, Cäcilia Freund 5 7, Anja Furtwängler 4 5 7, Nuno Filipe Gomes Martins 5 7, Florian Knolle 5 7, Gunnar U Neumann 4 5 7, Anthi Tiliakou 4 5 7, Anagnostis Agelarakis 8, Maria Andreadaki-Vlazaki 9, Philip Betancourt 10, Birgitta P Hallager 11, Olivia A Jones 12, Olga Kakavogianni 13, Athanasia Kanta 14, Panagiotis Karkanas 15, Efthymia Kataki 9, Konstantinos Kissas 16, Robert Koehl 17, Lynne Kvapil 18, Joseph Maran 19, Photini J P McGeorge 20, Alkestis Papadimitriou 21, Anastasia Papathanasiou 22, Lena Papazoglou-Manioudaki 23, Kostas Paschalidis 23, Naya Polychronakou-Sgouritsa 24, Sofia Preve 9, Eleni-Anna Prevedorou 15 25, Gypsy Price 26, Eftychia Protopapadaki 9, Tyede Schmidt-Schultz 27, Michael Schultz 27 28, Kim Shelton 29, Malcolm H Wiener 30, Johannes Krause 31 32 33, Choongwon Jeong 34, Philipp W Stockhammer 35 36 37 38
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- PMID:36646948
- PMCID: PMC9911347
- DOI: 10.1038/s41559-022-01952-3
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Ancient DNA reveals admixture history and endogamy in the prehistoric Aegean
Eirini Skourtanioti et al. Nat Ecol Evol.2023 Feb.
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Abstract
The Neolithic and Bronze Ages were highly transformative periods for the genetic history of Europe but for the Aegean-a region fundamental to Europe's prehistory-the biological dimensions of cultural transitions have been elucidated only to a limited extent so far. We have analysed newly generated genome-wide data from 102 ancient individuals from Crete, the Greek mainland and the Aegean Islands, spanning from the Neolithic to the Iron Age. We found that the early farmers from Crete shared the same ancestry as other contemporaneous Neolithic Aegeans. In contrast, the end of the Neolithic period and the following Early Bronze Age were marked by 'eastern' gene flow, which was predominantly of Anatolian origin in Crete. Confirming previous findings for additional Central/Eastern European ancestry in the Greek mainland by the Middle Bronze Age, we additionally show that such genetic signatures appeared in Crete gradually from the seventeenth to twelfth centuries BC, a period when the influence of the mainland over the island intensified. Biological and cultural connectedness within the Aegean is also supported by the finding of consanguineous endogamy practiced at high frequencies, unprecedented in the global ancient DNA record. Our results highlight the potential of archaeogenomic approaches in the Aegean for unravelling the interplay of genetic admixture, marital and other cultural practices.
© 2023. The Author(s).
Conflict of interest statement
The authors declare no competing interests.
Figures
a, Geographical distribution of archaeological sites mentioned in the study annotated by period. Sites with smaller symbols of light outline refer to the published datasets that are co-analysed and follow the same symbol/colour scheme. Data obtained from the same site but different periods, are annotated with jittering points.b, The number of individuals analysed and their date range based on archaeological chronology or radiocarbon dating. Site names are abbreviated in three-letter capitalized identifiers as indicated in the labels. E, Early; M, Middle; L, Late. See also Supplementary Tables 2 and 3.
The arrows indicate the two major observed genetic shifts: from the Neolithic (N) to the EBA and from the MBA to the LBA. A zoom-in of coordinates for the Aegean samples is given and is subdivided by region (right). In every panel, the coordinates of the counterparts are plotted in the background in faded colours. The three-letter identifier of every individual is plotted as well. HG, hunter-gatherers; Epipal., Epipalaeolithic.
a, Ternary plot for a three-way admixture model of Aegean individuals using the distal sources of ceramic farmers from Western Anatolia, Western Iranian farmers from Ganj Dareh and the EEHG, all dating to about 6000 bc . Because qpAdm is based on allele frequency differences, modelling of individual targets has a lower resolution especially when the SNP coverage is low. A few of the Late-Final Neolithic (LN) and EBA individuals show additional ancestry related to Neolithic Western Iran. To better visualize the fluctuation or Iranian-like coefficients among the LN-E/MBA individuals, the Anatolian–Iranian axis is also provided separately for Crete and the mainland islands. Fitting models were chosen with a cutoff ofP ≥ 0.01, with only four individuals falling in the lower range (0.01 ≤ P < 0.05).b, Allele frequencies are averaged among all LN-EBA individuals from the southern mainland and all EMBA Cretan individuals and modelled using proximal in time and space source populations. For the former, a source proxy from the Eneolithic/BA Caucasus fits better than Anatolia, whereas the opposite holds for Crete. However, for the latter, the model becomes adequate with the inclusion of additional low contribution from Neolithic Iran.P values and standard errors of mean were calculated by the qpAdm program applying a likelihood ratio test and the 5 cM block jackknifing method, respectively. No correction for multiple testing has been made. See also Extended Data Fig. 1 and Supplementary Tables 4–7.
a, Estimated mean coefficient (coeff.) (±1 s.e.) of additional ancestry (WES-related) using as proxy a BA Central European population (‘Germany LN-EBA Corded Ware’). For every group we assumed local ancestry in the models using the ascending population from the corresponding area (that is, EMBA Crete, LN-EBA southern Greek mainland and islands or LN northern mainland (for Logkas). Newly reported LBA groups are annotated in blue letters. Before we applied the modelling on every ‘Site_Period’ group, we performed a test of cladality among all individuals which suggested substructure within the LBA site of Chania in Crete and resulted in three analysis groups. Overall, individuals from LBA Crete are distributed in three groups of non-overlapping WES-related ancestry estimations (A, B and C). Models are supported withP ≥ 0.05, with the exception of Tiryns_IA and Pylos withP = 0.02 and 0.04, respectively.b, Modelling results using the approach of rotating competing sources 2 in the right populations set (R11) (Supplementary Note 2) for Crete, the mainland and the islands. LowP values (<0.01) indicate poor fit of the tested model and are annotated in red. For these models, theP values are compared with the model fit without rotation of the sources. The gradual shift in Crete can be explained with admixture from the mainland but other proximal sources fit equally well.P values and standard errors of mean were calculated by the qpAdm program applying a likelihood ratio test and the 5 cM block jackknifing method, respectively. No correction for multiple testing has been made. See also Extended Data Fig. 2 and Supplementary Tables 8 and 9.
The most parsimonious relationship between MYG004 and MYG005 is given. See also Extended Data Fig. 4.
a, Inferred ROH per ancient Aegean individual. Results are plotted by area and the archaeological period/date of each individual is provided following the same symbol/colour scheme introduced in Fig. 1. Simulations and expectations for given parental relationships and demographic scenarios are given. For many individuals the ROH length distribution matches close-kin unions (first and second cousins).b, Combined histogram of ROH length from all close-union offspring cases from the ossuary of Hagios Charalambos at the Lasithi plateau in Crete, compared to expected densities for certain parental relationships. See also Figs. 5 and 6.c, Scatterplot of lower coverage samples (250,000–400,000 SNPs) with total length of inferred ROH indicates that hapROH can reliably estimate long ROH at lower thresholds (Methods).
LowP values (conventionally < 0.05) are interpreted as a poor fit of the model and as more than one stream of ancestries being needed to explain the pair. Solid-line squares annotate clusters of individuals that date to the same period and come from the same archaeological site. Dashed-line square annotates Early Bronze Age (EBA) individuals from the islands of Euboea, Aegina and Koufonisia in Cyclades. Results are plotted in decreasing chronological order (Neolithic-Iron Age). We applied R11 (Supplementary Note 2) as a set of reference populations (‘right pops’).P values were calculated by the qpWave program applying a likelihood ratio test. No correction for multiple testing was performed.
A. Test of streams of ancestry necessary to explain a pair of individuals from a set of reference populations for the Middle/Late Bronze Age and one Iron Age individual from Tiryns. We repeated the analysis presented in Extended Data Fig. 1 by adding to the set of reference populations (R11) ‘W. Eurasian Steppe En-BA’. This setting increased the rate of non-cladal pairs (P < 0.01; at least two streams of ancestry) only among individuals from Chania (XAN) and led us to analyse Chania in three subgroups.P values were calculated by the qpWave program applying a likelihood ratio test. No correction for multiple testing was performed.B. The PC1-PC2 coordinates from the Western Eurasian PCA displaying XAN individuals with their IDs. Those analysed separately are annotated in red letters (XAN014, XAN028 and XAN034 were grouped together and XAN030 apart).
A. Positive coefficients from ‘W. Eurasian Steppe En-BA’ in LBA-IA males were fitted (P ≥ 0.01) for most autosomes as well as chromosome X. WES-related ancestry estimated from the X chromosome was substantially lower compared to the autosomes, although only a few of these comparisons were significant (Z-score ≥ 3).B. The same analysis for the ‘eastern’ ancestry indicates no sex bias in admixture between the Late Neolithic and the Middle Bronze Age.P alues and standard errors of mean were calculated by the qpAdm program applying a likelihood ratio test and the 5 cM block jackknifing method, respectively. No correction for multiple testing was performed.
A. The pairwise differences (P0) were computed with READ and are plotted as ±2SE of the mean. The dashed line indicates the median value calculated from all pairwise comparisons used for normalization (baseline of unrelatedness). Dotted lines show the cutoffs for the classification to second and first degrees and identical/twins. Confidence intervals were calculated by the software and are indicated in gray shadows. Results are provided separately for sites with related individuals.B. READ results for Neolithic Aposelemis in comparison to other Aegean Neolithic sites from the Greek mainland and Western Anatolia (mean pairwise differences with ±2SE) suggest that the baseline of unrelatedness might be lower for the Aposelemis population, and normalization ofP0 produces lower cutoffs for close relatives (light-red lines). In this scenario, APO004 and APO028 are second-degree relatives. Because SNP ascertainment influencesP0 values, only individuals enriched for 1240K, orin silico genotyped on these SNPs were included.C. lcMLkin analysis. Scatterplot ofk0 againstr for sites displaying pairs of relatives. First and up to third-degree relatives from Mygdalia are distinguished by both methods, as well as several pairs from Hagios Charalambos and Chania.
The ROH histograms are plotted for every case separately along with the expected densities for given parental relationships.
For the three parental relatedness scenarios (half-siblings, first cousins and second cousins), 1000 offspring were simulated with the software pedsim (Methods). For comparison with Fig. 6b, the histogram of every panel was created after combining ten simulated individuals at different proportions. Histograms with all simulated first cousins, or 80% first cousins and 20% second cousins mostly closely match the histogram from the combined Hagios Charalambos individuals.
References
- Evans, J. D. Excavations in the Neolithic settlement of Knossos, 1957–60. Part I.Annu. Br. Sch. Athens59, 132–240 (1964).
- Maran, J.Kulturwandel auf dem griechischen Festland und den Kykladen im späten 3. Jahrtausend v. Chr (Habelt, 1998).
- Wiersma, C. & Voutsaki, S. (eds)Social Change in Aegean Prehistory (Oxbow Books, 2017).
- Weiss, H. inThe Oxford Handbook of the Archaeology of the Levant: c. 8000–332 BCE (ed. Killebrew, A. E.) 367–387 (Oxford Univ. Press, 2014).
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