Abstract
Genomic analyses of Neanderthals have previously provided insights into their population history and relationship to modern humans1,2,3,4,5,6,7,8, 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 Cave9,10 and 2 from Okladnikov Cave11—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.
Main
Neanderthals occupied western Eurasia from around 430,000 years ago8,12 until their extinction around 40,000 years ago13. Genome-scale data have been reported for the skeletal remains of 18 individuals from 14 archaeological sites1,2,3,4,5,6,7,8 spanning Neanderthal history across large parts of their known geographical range, which extends as far east as the Altai Mountains in southern Siberia. These data have yielded a broad overview of Neanderthal populations, indicating the existence of multiple distinct Neanderthal populations over time and space1,2,14.
However, little is known about the genetic relationships and social organization within and between Neanderthal communities in any part of Eurasia during this time interval.
By ‘social organization’, we mean the size, sex composition and spatiotemporal cohesion of a community15. We define a community as a set of individuals that presumably lived together at the same location, and reserve the term population for a broadly connected set of communities in a wider geographical area.
On the basis of fossilized footprints16,17 and spatial patterns of site use18, previous studies on the social organization of Neanderthal communities have suggested that Neanderthals probably lived in small communities. In addition, partial mitochondrial DNA (mtDNA) sequences from six adult Neanderthals have been used to suggest that Neanderthals may have been patrilocal19, although this suggestion has been debated20.
Here we explore the social organization of Neanderthals using nuclear, Y-chromosomal and mtDNA data from the remains of 13 individuals recovered from 2 sites located close to one another in southern Siberia (Russia)—Chagyrskaya and Okladnikov caves (Table 1 and Fig. 1a).
Archaeological sites and remains
The Chagyrskaya and Okladnikov caves, located in the foothills of the Altai Mountains (Fig. 1a and Extended Data Figs. 1 and 2), are thought to have been used mainly as short-term hunting camps11,21. They are two of three known sites at which a distinctive Sibiryachikha Middle Palaeolithic industry has been found (the third being Upper Sibiryachikha Cave)9,10,22,23 (Supplementary Fig. 1.6). The Sibiryachikha industry at Chagyrskaya and Okladnikov caves is distinct from the Middle Palaeolithic industry at Denisova Cave (located around 100 km to the east), where Neanderthal remains have also been found2.
The Neanderthal occupation deposits at Chagyrskaya Cave accumulated between 59,000 and 51,000 years ago, as indicated by optical dating of sediments and radiocarbon dating of bison bones10. We obtained additional radiocarbon ages from two pieces of charcoal and a Neanderthal bone (Chagyrskaya 9), all of which were older than 50,000 years before present (Supplementary Table 1.3). These ages are compatible with a short period of deposition (a few millennia or less), which is consistent with the presence of similar archaeological industry in all Neanderthal layers10 (Extended Data Fig. 2).
For Okladnikov Cave, we constrained the timing of Neanderthal occupation using hydroxyproline-based single amino-acid radiocarbon ages for three Neanderthal specimens (including Okladnikov 15) (Table 1 and Extended Data Table 1), which indicated that they were at least 44,000 years old (Supplementary Table 1.4). Our age estimates are consistent with uranium-series ages for animal bones and support previous suggestions that younger radiocarbon ages obtained from the collagen fraction reflect an incomplete removal of contaminants24 (Supplementary Information section 1). Therefore, the archaeological and chronological data suggest that the Neanderthals that occupied these two sites may have been broadly contemporaneous.
Previous analyses of high-coverage genomes of a Neanderthal from Chagyrskaya Cave (Chagyrskaya 8) and an earlier Neanderthal from Denisova Cave (Denisova 5, the ‘Altai Neanderthal’) revealed that they belonged to different populations5. A first-generation offspring (Denisova 11) of a Neanderthal mother and a Denisovan father revealed that the Neanderthal mother was more similar to Chagyrskaya 8 than she was to other Neanderthals5,25.
Data acquisition and sex determination
We sampled 1–64 mg of tooth or bone powder from 17 specimens from Chagyrskaya Cave and 10 specimens from Okladnikov Cave. Of these, 15 from Chagyrskaya and 2 from Okladnikov yielded ancient DNA (Table 1, Extended Data Table 1 and Supplementary Data 1), from which we generated a total of 85 single-stranded DNA libraries (Supplementary Information section 2). All of the libraries were enriched for mtDNA sequences (Supplementary Information section 3) and 49 libraries (selected for high sequence yields and low levels of present-day human contamination) were enriched for nuclear DNA using a newly designed nuclear-capture array containing 643,472 transversion polymorphisms across the genome (Supplementary Information section 5). In the array, 271,306 sites vary among the 4 published high-coverage archaic individuals (three Neanderthals and one Denisovan)2,3,5,14 and 372,166 sites segregate in present-day African populations or are fixed between present-day humans and archaic hominins. The average nuclear DNA coverage for each fossil ranges from 0.04- to 12.3-fold (Fig. 1b), and present-day human contamination estimates range from 0.1% to 3.2% (Supplementary Table 5.4).
We determined the genetic sex of the 17 remains using the difference in coverage between the X chromosome and autosomes (Supplementary Fig. 5.5) and found that 6 remains stemmed from females. For the 11 male remains, we enriched the libraries for around 6.9 megabases (Mb) of Y-chromosome sequence26 (Supplementary Information section 4), yielding coverages ranging between 0.02- and 42.2-fold (Supplementary Table 4.3).
Identification of relatives
To determine whether any of the remains originated from related individuals, we computed the nuclear DNA divergence between the 17 remains by randomly sampling 1 allele from 250,785 sites in the capture array that were variable in the high-coverage archaic individuals (excluding variants specific to Chagyrskaya 8) (Supplementary Information section 5)….
