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Genetic insights into the social organization of Neanderthals

Skov, Laurits, Peyrégne, Stéphane, Popli, Divyaratan, Iasi, Leonardo N. M., Devièse, Thibaut, Slon, Viviane, Zavala, Elena I., Hajdinjak, Mateja, Sümer, Arev P., Grote, Steffi, Bossoms Mesa, Alba, López Herráez, David, Nickel, Birgit, Nagel, Sarah, Richter, Julia, Essel, Elena, Gansauge, Marie, Schmidt, Anna, Korlević, Petra, Comeskey, Daniel, Derevianko, Anatoly P., Kharevich, Aliona, Markin, Sergey V., Talamo, Sahra, Douka, Katerina, Krajcarz, Maciej T., Roberts, Richard G., Higham, Thomas, Viola, Bence, Krivoshapkin, Andrey I., Kolobova, Kseniya A., Kelso, Janet, Meyer, Matthias, Pääbo, Svante, Peter, Benjamin M.·2022·Nature
DOI 10.1038/s41586-022-05283-yPMC PMC9581778
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Abstract

Genomic analyses of Neanderthals have previously provided insights into their population history and relationship to modern humans 1–8 , but the social organization of Neanderthal communities remains poorly understood. Here we present genetic data for 13 Neanderthals from two Middle Palaeolithic sites in the Altai Mountains of southern Siberia: 11 from Chagyrskaya Cave 9,10 and 2 from Okladnikov Cave 11 —making this one of the largest genetic studies of a Neanderthal population to date. We used hybridization capture to obtain genome-wide nuclear data, as well as mitochondrial and Y-chromosome sequences. Some Chagyrskaya individuals were closely related, including a father–daughter pair and a pair of second-degree relatives, indicating that at least some of the individuals lived at the same time. Up to one-third of these individuals’ genomes had long segments of homozygosity, suggesting that the Chagyrskaya Neanderthals were part of a small community. In addition, the Y-chromosome diversity is an order of magnitude lower than the mitochondrial diversity, a pattern that we found is best explained by female migration between communities. Thus, the genetic data presented here provide a detailed documentation of the social organization of an isolated Neanderthal community at the easternmost extent of their known range.

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Fig. 1 Neanderthal sites and genomic information. a, Locations of all of the sites with Neanderthal remains (the number of individuals is given in parentheses for sites with multiple individuals) from whom nuclear DNA has been extracted, with a close-up of the Chagyrskaya and Okladnikov caves in the Altai region of southern Siberia. b, Nuclear genomes ranked by the extent of coverage and colour-coded by site (blue, Chagyrskaya from this study; orange, Okladnikov from this study; grey, published previously in refs. 1–8). c, Maximum-likelihood tree for mtDNA sequences from the Neanderthal individuals included in this study in the context of known hominin variation. The reference genome is rCRS and the accession numbers for the present-day humans are East Asian (AF346973), European (AF346981) and African (AF381988). Okladnikov 2 refers to the mtDNA sequence in ref. 41 (this specimen is listed as Okladnikov 14 in Extended Data Table 1). Data from refs. 1–4,6,30,41,42–49. d, Maximum-likelihood tree based on consensus calling of 6.9 Mb of the Y chromosome of four Chagyrskaya individuals with coverage of more than onefold, along with previously published Y-chromosome data from three Neanderthals, two Denisovans and four present-day humans. The reference genome is hg19. Data from refs. 26,50–53. In c and d, the haplogroups are shown for present-day human populations.
Fig. 1 Neanderthal sites and genomic information. a, Locations of all of the sites with Neanderthal remains (the number of individuals is given in parentheses for sites with multiple individuals) from whom nuclear DNA has been extracted, with a close-up of the Chagyrskaya and Okladnikov caves in the Altai region of southern Siberia. b, Nuclear genomes ranked by the extent of coverage and colour-coded by site (blue, Chagyrskaya from this study; orange, Okladnikov from this study; grey, published previously in refs. 1–8). c, Maximum-likelihood tree for mtDNA sequences from the Neanderthal individuals included in this study in the context of known hominin variation. The reference genome is rCRS and the accession numbers for the present-day humans are East Asian (AF346973), European (AF346981) and African (AF381988). Okladnikov 2 refers to the mtDNA sequence in ref. 41 (this specimen is listed as Okladnikov 14 in Extended Data Table 1). Data from refs. 1–4,6,30,41,42–49. d, Maximum-likelihood tree based on consensus calling of 6.9 Mb of the Y chromosome of four Chagyrskaya individuals with coverage of more than onefold, along with previously published Y-chromosome data from three Neanderthals, two Denisovans and four present-day humans. The reference genome is hg19. Data from refs. 26,50–53. In c and d, the haplogroups are shown for present-day human populations.CC BY · PubMed Central
Fig. 2 Genomic diversity for Chagyrskaya Neanderthals compared with other hominids. Neanderthal (blue), early modern human (orange) and present-day gorilla (green) populations are coloured the same throughout the figure. Present-day human populations are coloured according to the geographical region (see colour key). a, The proportion of the genome that is in homozygous tracts longer than 10 cM (dark) and tracts between 2.5 and 10 cM (light colour) for ancient individuals (early modern humans, Neanderthals and Denisovans). b, Average proportion of the genome that is homozygous for Chagyrskaya Neanderthals, early modern humans (grouped together) and present-day human and gorilla populations37. Data are mean ± 95% confidence intervals for the estimates of the mean. The sample size is equal to that of the mtDNA sequences listed below. c, Mean coalescence time for mtDNA (MT) and Y chromosome (left and right bars of each pair, respectively) for Neanderthal, early modern human and gorilla populations. d, Mean coalescence time for early modern humans (grouped together) and present-day human and gorilla populations. c,d, Data are mean ± 95% confidence intervals and points are all pairwise comparisons. The number of Y chromosome and mtDNA-genomes used in pairwise comparisons for each population is as follows: Neanderthal and Denisovan, Chagyrskaya (MT = 12, Y = 6), Vindija (MT = 4, Y = 0), Goyet (Neanderthal) (MT = 7, Y = 0); early modern humans, Sunghir (MT = 4, Y = 4), Věstonice (MT = 4, Y = 0), Goyet (MT = 5, Y = 0), Bacho Kiro (MT = 4, Y = 3), which combined is (MT = 17, Y = 7); gorillas, mountain gorilla (MT = 8, Y = 3), eastern lowland gorilla (MT = 7, Y = 2); Americas, Suruí (MT = 9, Y = 4), Karitiana (MT = 13, Y = 5), Pima (MT = 14, Y = 7), Colombian (MT = 8, Y = 2), Mayan (MT = 22, Y = 2); central South Asia, Balochi (MT = 25, Y = 24), Makrani (MT = 26, Y = 20), Pathan (MT = 25, Y = 19), Sindhi (MT = 25, Y = 20), Brahui (MT = 26, Y = 25); Europe, French (MT = 29, Y = 11), Basque (MT = 24, Y = 15), Adygei (MT = 17, Y = 7), Sardinian (MT = 29, Y = 15), Russian (MT = 26, Y = 16); East Asia, Lahu (MT = 9, Y = 7), Japanese (MT = 28, Y = 19), Yakut (MT = 26, Y = 18), Han (MT = 34, Y = 15), Naxi (MT = 9, Y = 6); Africa, Biaka (MT = 23, Y = 22), Mbuti (MT = 14, Y = 10), Yoruba (MT = 23, Y = 11), Mandinka (MT = 23, Y = 14), Bantu (Kenya) (MT = 12, Y = 10).
Fig. 2 Genomic diversity for Chagyrskaya Neanderthals compared with other hominids. Neanderthal (blue), early modern human (orange) and present-day gorilla (green) populations are coloured the same throughout the figure. Present-day human populations are coloured according to the geographical region (see colour key). a, The proportion of the genome that is in homozygous tracts longer than 10 cM (dark) and tracts between 2.5 and 10 cM (light colour) for ancient individuals (early modern humans, Neanderthals and Denisovans). b, Average proportion of the genome that is homozygous for Chagyrskaya Neanderthals, early modern humans (grouped together) and present-day human and gorilla populations37. Data are mean ± 95% confidence intervals for the estimates of the mean. The sample size is equal to that of the mtDNA sequences listed below. c, Mean coalescence time for mtDNA (MT) and Y chromosome (left and right bars of each pair, respectively) for Neanderthal, early modern human and gorilla populations. d, Mean coalescence time for early modern humans (grouped together) and present-day human and gorilla populations. c,d, Data are mean ± 95% confidence intervals and points are all pairwise comparisons. The number of Y chromosome and mtDNA-genomes used in pairwise comparisons for each population is as follows: Neanderthal and Denisovan, Chagyrskaya (MT = 12, Y = 6), Vindija (MT = 4, Y = 0), Goyet (Neanderthal) (MT = 7, Y = 0); early modern humans, Sunghir (MT = 4, Y = 4), Věstonice (MT = 4, Y = 0), Goyet (MT = 5, Y = 0), Bacho Kiro (MT = 4, Y = 3), which combined is (MT = 17, Y = 7); gorillas, mountain gorilla (MT = 8, Y = 3), eastern lowland gorilla (MT = 7, Y = 2); Americas, Suruí (MT = 9, Y = 4), Karitiana (MT = 13, Y = 5), Pima (MT = 14, Y = 7), Colombian (MT = 8, Y = 2), Mayan (MT = 22, Y = 2); central South Asia, Balochi (MT = 25, Y = 24), Makrani (MT = 26, Y = 20), Pathan (MT = 25, Y = 19), Sindhi (MT = 25, Y = 20), Brahui (MT = 26, Y = 25); Europe, French (MT = 29, Y = 11), Basque (MT = 24, Y = 15), Adygei (MT = 17, Y = 7), Sardinian (MT = 29, Y = 15), Russian (MT = 26, Y = 16); East Asia, Lahu (MT = 9, Y = 7), Japanese (MT = 28, Y = 19), Yakut (MT = 26, Y = 18), Han (MT = 34, Y = 15), Naxi (MT = 9, Y = 6); Africa, Biaka (MT = 23, Y = 22), Mbuti (MT = 14, Y = 10), Yoruba (MT = 23, Y = 11), Mandinka (MT = 23, Y = 14), Bantu (Kenya) (MT = 12, Y = 10).CC BY · PubMed Central
Extended Data Fig. 1 Chagyrskaya and Okladnikov Caves. A, Location map of Chagyrskaya and Okladnikov Caves in the Altai region of southern Siberia. Views of the B, north-facing entrance to Chagyrskaya Cave and C, south-facing entrance to Okladnikov Cave.
Extended Data Fig. 1 Chagyrskaya and Okladnikov Caves. A, Location map of Chagyrskaya and Okladnikov Caves in the Altai region of southern Siberia. Views of the B, north-facing entrance to Chagyrskaya Cave and C, south-facing entrance to Okladnikov Cave.CC BY · PubMed Central
Extended Data Fig. 2 Plan map of Chagyrskaya Cave and locations of Neanderthal remains. A, Spatial distribution of Neanderthal remains. The excavated area is shown in grey, and the blue line (transect A–B) marks the position of the stratigraphic profile shown in B. The coloured squares and ellipses denote Neanderthal remains located with exact coordinates or within the circumscribed areas, respectively, and are annotated with the corresponding fossil number(s). B, Stratigraphic profile along transect A–B in A. Locations of Neanderthal remains are projected orthogonally onto this profile, so each fossil is not necessarily shown in the stratigraphic unit from which it was recovered.
Extended Data Fig. 2 Plan map of Chagyrskaya Cave and locations of Neanderthal remains. A, Spatial distribution of Neanderthal remains. The excavated area is shown in grey, and the blue line (transect A–B) marks the position of the stratigraphic profile shown in B. The coloured squares and ellipses denote Neanderthal remains located with exact coordinates or within the circumscribed areas, respectively, and are annotated with the corresponding fossil number(s). B, Stratigraphic profile along transect A–B in A. Locations of Neanderthal remains are projected orthogonally onto this profile, so each fossil is not necessarily shown in the stratigraphic unit from which it was recovered.CC BY · PubMed Central
Extended Data Fig. 3 Normalized pairwise differences between Chagyrskaya and Okladnikov remains. A, Points show the mean pairwise differences (y-axis) between two remains (normalized by the median difference between all pairs of remains). Remains that were identified as identical, first degree and second degree relatives are named (x-axis shows the first fossil and the number denotes the second remain). Error bars are 95% confidence intervals for 100 bootstrap estimates of the mean pairwise differences. Horizontal lines indicate the expected normalized difference for identical individuals, first degree relationships, second degree relationships and unrelated individuals27. B, Each circle/square represents an individual (blue for Chagyrskaya, orange for Okladnikov) and the small white circles indicate which remains originated from this individual. The black circle for Chagyrskaya 8 indicates that the genomic sequence for this bone is previously published. Squares indicate that the individual is male and circles indicate that the individual is female. Individuals which are first degree relatives, second degree relatives or share heteroplasmies are marked.
Extended Data Fig. 3 Normalized pairwise differences between Chagyrskaya and Okladnikov remains. A, Points show the mean pairwise differences (y-axis) between two remains (normalized by the median difference between all pairs of remains). Remains that were identified as identical, first degree and second degree relatives are named (x-axis shows the first fossil and the number denotes the second remain). Error bars are 95% confidence intervals for 100 bootstrap estimates of the mean pairwise differences. Horizontal lines indicate the expected normalized difference for identical individuals, first degree relationships, second degree relationships and unrelated individuals27. B, Each circle/square represents an individual (blue for Chagyrskaya, orange for Okladnikov) and the small white circles indicate which remains originated from this individual. The black circle for Chagyrskaya 8 indicates that the genomic sequence for this bone is previously published. Squares indicate that the individual is male and circles indicate that the individual is female. Individuals which are first degree relatives, second degree relatives or share heteroplasmies are marked.CC BY · PubMed Central
Extended Data Fig. 4 Sharing of variants among archaic genomes. The center of the errorbar show the D-statistic of the form D((Denisova 5/Vindija33.19), Chagyrskaya 8; Test, Chimpanzee) and error bars are the corresponding 95% confidence intervals calculated for 643,472 SNPs using a weighted block jackknife and a block size of 5 Mb. Points with |Z-score| > 2 are annotated with an asterisk. The dashed vertical line is at D = 0. Note that Chagyrskaya F is the same individual as Chagyrskaya 8 and VindijaG1 is the same individual as Vindija 33.19.
Extended Data Fig. 4 Sharing of variants among archaic genomes. The center of the errorbar show the D-statistic of the form D((Denisova 5/Vindija33.19), Chagyrskaya 8; Test, Chimpanzee) and error bars are the corresponding 95% confidence intervals calculated for 643,472 SNPs using a weighted block jackknife and a block size of 5 Mb. Points with |Z-score| > 2 are annotated with an asterisk. The dashed vertical line is at D = 0. Note that Chagyrskaya F is the same individual as Chagyrskaya 8 and VindijaG1 is the same individual as Vindija 33.19.CC BY · PubMed Central
Extended Data Fig. 5 Deletion of the AMELY gene on the Y-chromosome. Deletion of 1.8 Mb of sequence on the Y-chromosome of Mezmaiskaya 2 (bottom panel, light grey) compared to Chagyrskaya D (top panel, no deletion). The horizontal axis shows the genomic position on the Y-chromosome and the vertical axis shows the coverage in bins of 10 kb, normalized by the chromosome-wide average coverage. Bin colours indicate the region classes on the human reference Y-chromosome, with darker regions indicating coverage by the Y-chromosome capture array. Black bars denote known coding genes.
Extended Data Fig. 5 Deletion of the AMELY gene on the Y-chromosome. Deletion of 1.8 Mb of sequence on the Y-chromosome of Mezmaiskaya 2 (bottom panel, light grey) compared to Chagyrskaya D (top panel, no deletion). The horizontal axis shows the genomic position on the Y-chromosome and the vertical axis shows the coverage in bins of 10 kb, normalized by the chromosome-wide average coverage. Bin colours indicate the region classes on the human reference Y-chromosome, with darker regions indicating coverage by the Y-chromosome capture array. Black bars denote known coding genes.CC BY · PubMed Central
Extended Data Fig. 6 Ratios of mitochondrial DNA to Y-chromosome diversity. Black circles indicate mean estimates for each population and error bars are the corresponding 95% confidence intervals using 100 bootstrap iterations. Negative values denote lower Y-chromosome diversity than mitochondrial (mt) DNA diversity.
Extended Data Fig. 6 Ratios of mitochondrial DNA to Y-chromosome diversity. Black circles indicate mean estimates for each population and error bars are the corresponding 95% confidence intervals using 100 bootstrap iterations. Negative values denote lower Y-chromosome diversity than mitochondrial (mt) DNA diversity.CC BY · PubMed Central

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Metadata

Authors
Skov, L., Peyrégne, S., Popli, D., Iasi, L. N. M., Devièse, T., Slon, V., Zavala, E. I., Hajdinjak, M., Sümer, A. P., Grote, S., Bossoms Mesa, A., López Herráez, D., Nickel, B., Nagel, S., Richter, J., Essel, E., Gansauge, M., Schmidt, A., Korlević, P., Comeskey, D., Derevianko, A. P., Kharevich, A., Markin, S. V., Talamo, S., Douka, K., Krajcarz, M. T., Roberts, R. G., Higham, T., Viola, B., Krivoshapkin, A. I., Kolobova, K. A., Kelso, J., Meyer, M., Pääbo, S., & Peter, B. M.
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2022-10-19
Volume
610
Issue
7932
Pages
519-525
ISSN
  • 0028-0836
  • 1476-4687
DOI
10.1038/s41586-022-05283-y
PMC
PMC9581778
Cited by
106
References
14
Language
en
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