The value of dirty DNA
Environmental DNA can identify the presence of species, even from the distant past. Surveying three cave sites in western Europe and southern Siberia, Vernot et al. identified nuclear DNA and confirmed that it is from the close relatives of anatomically modern humansNeanderthal and Denisovan individuals. A phylogenetic analysis and modeling show that the DNA in sediment samples from several layers corresponds to previously studied skeletal remains. These results demonstrate that environmental data can be applied to study the population genetics of the extinct Neanderthal and Denisovan lineages, identifying a turnover of Neanderthal populations 100,000 years ago.
Science, this issue p. eabf1667
The study of hominin history has progressed through both archaeological and genetic insights. Although DNA sequencing from hominin skeletal remains allows the association of ancient populations with specific places in time and space, many archaeological sites lack associated hominin remains, limiting the scope of genetic analyses. Even when ancient hominin remains are found, they often do not cover the full time span of a site or sampling them for DNA may not be possible. The fossil record is particularly sparse for Pleistocene hominins, leaving large gaps in our understanding of the genetic histories of archaic and early modern humans.
Recent work has demonstrated the feasibility of sequencing ancient mammalian mitochondrial DNA (mtDNA), including that of hominins, from Pleistocene cave sediments. However, mtDNA represents only the maternal lineage and thus provides limited data for the resolution of population relationships. It is therefore desirable to complement mtDNA analysis with the retrieval of nuclear DNA, but no strategies are in place to enrich hominin nuclear DNA from a background of related sequences from other mammals present in most sedimentary deposits. To close this gap, we developed a set of probes for hybridization capture that targets 1.6 million ancestry-informative positions in the hominin nuclear genome, specifically at loci with high mammalian sequence divergence. We then developed computational methods to deplete residual microbial and faunal DNA sequences, along with methods to account for such non-hominin DNA in population genetic analyses.
We applied these methods to explore the history of Neanderthal populations in western Europe and southern Siberia using sediment samples from three Pleistocene caves: Galera de las Estatuas, a site in northern Spain with 40 thousand years of Neanderthal occupation but that is genetically unexplored, and Chagyrskaya and Denisova Caves, which have previously yielded high-coverage genomes of two Neanderthals and one Denisovan hominin. In total, we recovered Neanderthal or Denisovan mtDNA from >60 sediment samples and nuclear DNA from 30 of these. For Chagyrskaya and Denisova Caves, our phylogenetic results from sediment DNA were consistent with previously published results from skeletal remains, confirming the accuracy of our approach. At Galera de las Estatuas, we recovered Neanderthal DNA from layers spanning nearly the entire stratigraphy, and identified a population turnover ~100,000 years ago accompanied by a loss of mtDNA diversity. By incorporating genetic data from previously published skeletal samples, we associated this turnover with two putative radiations in Neanderthal history.
We developed methods for the effective retrieval and analysis of ancient hominin nuclear DNA from sediments and used them to uncover previously unknown events in Neanderthal history. This work demonstrates that detailed genetic analyses are now possible for many more archaeological sites than previously thought, with DNA from abundant sediments allowing dense time-series studies that are independent of the fossil record.
Shown is a view of pit I at the Galera de las Estatuas, Spain, and stratigraphic column with ages in thousands of years (ka).
Bones and teeth are important sources of Pleistocene hominin DNA, but are rarely recovered at archaeological sites. Mitochondrial DNA (mtDNA) has been retrieved from cave sediments but provides limited value for studying population relationships. We therefore developed methods for the enrichment and analysis of nuclear DNA from sediments and applied them to cave deposits in western Europe and southern Siberia dated to between 200,000 and 50,000 years ago. We detected a population replacement in northern Spain about 100,000 years ago, which was accompanied by a turnover of mtDNA. We also identified two radiation events in Neanderthal history during the early part of the Late Pleistocene. Our work lays the ground for studying the population history of ancient hominins from trace amounts of nuclear DNA in sediments.
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