Long genetic and social isolation in Neanderthals before their extinction

Slimak, L., Vimala, T., Seguin-Orlando, A., Metz, L., Zanolli, C., Joannes-Boyau, R., Frouin, M., Arnold, L.J., Demuro, M., Devièse, T., Comeskey, D., Buckley, M., Camus, H., Muth, X., Lewis, J.E., Bocherens, H., Yvorra, P., Tenailleau, C., Duployer, B., Coqueugniot, H., Dutour, O., Higham, T., Sikora, M., 2024. Long genetic and social isolation in Neanderthals before their extinction. Cell Genomics 4.

INTRODUCTION
Multiple theories have been presented over the years to address the Neanderthals’ extinction 40 thousand years ago. These approaches are commonly based on the identification of various incidents, ranging from climatic changes to volcanic eruptions or magnetic field reversals. They are thus attributed to ecological factors, implying that the Neanderthals’ extinction was more the result of natural events of external origin rather than of processes related to the biological and cultural features of these populations themselves. Internal causes, based on the social, historical, or ethological structures of Neanderthal populations, remain largely underexplored. 1–7 It should be noted that paleogenomic and osteological studies have revealed low effective population sizes and signatures of inbreeding in Siberian and late European Neanderthals, 7–9 suggesting social structures characterized by small group sizes and low intergroup mobility.

This contrasts with recent results from early Eurasian modern humans, which showed low levels of inbreeding and higher intergroup mobility despite small group sizes. 9,10 Whether these results are representative of wider Neanderthal and modern human social organization remains inconclusive.
Since the publication of the first draft of the Neanderthal genome in 2010, 11 Neanderthal genomes have been recovered from sites across Eurasia, painting an increasingly complex picture of Neanderthal genetic structure. The deepest divergence among Neanderthal genomes sequenced to date is found between eastern and western Eurasian Neanderthal populations represented by the 120 kiloannum (ka) Altai Neanderthal from Denisova Cave 8 and the >44 ka Vindija 33.19 individual from Croatia. 12 Genomic data of all other available Neanderthal remains, the earliest in western Europe being 120 ka (Scladina and Hohlenstein-Stadel [HST]), while the latest being 40 ka, suggest genetic continuity in western Eurasia for 80 ka. 13

Recent results obtained from sedimentary DNA suggest that the genetic landscape was significantly altered by expansions of Neanderthal populations 105 ka. 14 This gave rise to lineages in Europe represented by samples from central Europe (Vindija), the Caucasus (Mezmaiskaya Cave), and Siberia (Chagyrskaya Cave 8), 15 the latter likely replacing the earlier Altai-like population. The genomes of late (<50 ka) European Neanderthals, including an individual from the Caucasus (Mezmaiskaya 2), were found to be more similar to Vindija than to other known lineages, indicating further population turnover toward the last stages of Neanderthal history in the Caucasus or western Europe. 16 The close correlation between genetic similarities and geographic location suggested an absence of major population structure among the sampled late Neanderthal populations. It remains unknown whether these patterns result from long-term in situ evolution of late European Neanderthal populations or as a consequence of a recent expansion of Vindija-like lineages into Europe.

Here, we report the discovery of a late Neanderthal individual, nicknamed ‘‘Thorin,’’ in 2015, and progressively excavated since then at Grotte Mandrin in Mediterranean France, a site that also was temporarily occupied by early modern humans at 54 ka. 1 Thorin is one of the best-represented Neanderthal individuals found in France since the discovery from Saint-Ce´ saire in 1979. 17 Combining archaeological, chronostratigraphic, isotopic, and genomic analyses, we show that Thorin belonged to a late Neanderthal population that had stayed genetically isolated for 50 ka. Separate from the Thorin lineage, we find evidence of gene flow from another lineage, which diverged from the ancestral lineage of the European Neanderthals >80 ka, in the genome of the Les Cotte´ s Neanderthal. 16 Our results suggest the presence of multiple isolated late Neanderthal communities in Europe close to their time of extinction and shed light on their social organization, with limited, if any, level of interactions between different Neanderthal populations in their last millennia, even though these populations were geographically very close to each other.

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