Genetic diversity of late Neanderthals in northwestern Europe

Genetic diversity of late Neanderthals in northwestern Europe

Archaeological, osteological and genetic evidence suggests that Neanderthals lived in small groups; however, less is known about whether these groups were part of isolated communities or belonged to larger, well-connected populations. The dense concentration of broadly contemporaneous Neanderthal sites in the Meuse Basin, Belgium, provides a rare opportunity to study regional populations at high resolution. Here we generated genetic data from twenty-seven Neanderthals who lived less than approximately fifty-two thousand five hundred years ago from ten archaeological sites in Belgium and France, including a high-coverage genome from a forty-five thousand-year-old individual from Goyet, Belgium. We show that most of these individuals are more closely related to one another than to other contemporaneous late Neanderthals in Europe. Further, some of these individuals carry DNA from a Neanderthal lineage predating the split of late Neanderthals. Although these Neanderthals overlapped temporally with early modern humans in northwestern Europe from around forty-seven thousand years ago, we find no evidence of recent gene flow from modern humans. They also do not show the genetic signatures of mating among close relatives found in Altai Neanderthals, suggesting that they lived in larger or better-connected groups. Moreover, genetic load did not accumulate over time, arguing against progressive genetic deterioration as a driver of Neanderthal extinction.

Neanderthals lived in Europe and western Asia from at least around four hundred thirty thousand years ago until around forty thousand years before present. The high-quality nuclear genomes of four Neanderthals provided numerous insights into the diversity and population history of Neanderthals and their interactions with early modern humans. The more recent Vindija thirty-three point one nine Neanderthal from Croatia, approximately forty-five thousand years before present, shows higher genetic diversity and less evidence of recent inbreeding than do the older Neanderthals from Denisova and Chagyrskaya caves, Altai Neanderthal, approximately one hundred twenty thousand years before present; Denisova seventeen, approximately one hundred ten thousand years before present; and Chagyrskaya eight, approximately sixty thousand years before present, who lived in the easternmost part of the known Neanderthal range. Further lower-coverage nuclear genomes from four late Neanderthals suggest close genetic affinities between individuals from geographically distant regions, such as Mezmaiskaya, Caucasus, Russia, and Les Cottés, Poitou, France, indicating possible long-range connectivity between late Neanderthals.

Pleistocene remains are rare with generally low DNA preservation, but recent methodological advances-including microsampling, improved decontamination, extraction, library preparation and enrichment methods-have improved the recovery of degraded DNA, enabling studies of larger numbers of Neanderthal remains. The low-coverage genomes of eleven Neanderthals from Chagyrskaya Cave revealed patterns of close kinship and low genetic diversity. However, because these observations are based on a single group at the eastern periphery of the Neanderthal range, the extent to which such findings are representative of Neanderthal diversity and population structure in general remains open.

A new fine-scale dataset

The Meuse Basin in Belgium offers a unique opportunity to study broadly contemporaneous late Neanderthals owing to its high concentration of Middle Palaeolithic sites. Most of these sites were excavated during the nineteenth century, complicating the secure association with lithic assemblages and making their reliable contextualization more challenging. Recent efforts, including reanalysis of faunal collections, identified further Neanderthal remains resulting in fourteen new Neanderthal mitochondrial genomes from the region, including from Troisième Caverne of Goyet, Spy, Fonds-de-Forêt, Scladina and Trou Magrite, and three low-coverage nuclear genomes of Neanderthals from Scladina, I4-A, Spy, ninety-four a, and Goyet, Q56-one, which

Information section 1). Most of these sites were excavated during the nineteenth century, complicating the secure association with lithic assemblages and making their reliable contextualization more chal- lenging4. Recent efforts, including reanalysis of faunal collections, identified further Neanderthal remains19-22 resulting in 14 new Nean- derthal mitochondrial genomes from the region (including from Troisième Caverne of Goyet, Spy, Fonds-de-Forêt, Scladina and Trou Magrite)4,11,21,23,24 and three low-coverage nuclear genomes of Neander- thals from Scladina (I4-A)23, Spy (94a) and Goyet (Q56-1 (ref. 11)), which showed that the Spy ninety-four a and Goyet Q56-one individuals share significantly more derived alleles with each other than with any other late Neanderthal sequenced to date.

However, key aspects of Neanderthal population structure in this region remain unexplored. Morphology-based analyses estimate that eighty Neanderthal remains from Spy and one hundred one remains from Goyet belonged to at least three and six individuals, respectively, but the exact numbers remain unclear. Despite their genetic similarity, mortuary practices of the Neanderthals from Spy and Goyet are very different. At Spy, the anatomical connection between the bones suggests deliberate burial, although this interpretation has been questioned. By contrast, the Neanderthal remains at Goyet are highly fragmented, with anthropogenic modifications suggesting that the individuals were cannibalized. Together with evidence for contrasting mobility patterns, sulfur isotope values suggest local foraging at Spy but non-local origins at Goyet, this points to greater diversity among late Neanderthals in northwestern Europe than is at present evident from genetic data.

Many of the sites in the Meuse Basin and surrounding areas have yielded Neanderthal remains dated to around forty-five thousand years before present or more recently, a time when modern humans were already present in central Europe. However, the radiocarbon dates of bone implements recovered from the archaeological sites in Belgium suggest that there was no overlap between modern humans and Neanderthals in this region. Obtaining genetic data from both Neanderthals and modern humans could help to resolve this question, as direct evidence of recent mixture between them would establish an overlap.