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. 2019 Jul 30;116(31):15610-15615.
doi: 10.1073/pnas.1903984116. Epub 2019 Jul 15.

A Genetic Analysis of the Gibraltar Neanderthals

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Free PMC article

A Genetic Analysis of the Gibraltar Neanderthals

Lukas Bokelmann et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

The Forbes' Quarry and Devil's Tower partial crania from Gibraltar are among the first Neanderthal remains ever found. Here, we show that small amounts of ancient DNA are preserved in the petrous bones of the 2 individuals despite unfavorable climatic conditions. However, the endogenous Neanderthal DNA is present among an overwhelming excess of recent human DNA. Using improved DNA library construction methods that enrich for DNA fragments carrying deaminated cytosine residues, we were able to sequence 70 and 0.4 megabase pairs (Mbp) nuclear DNA of the Forbes' Quarry and Devil's Tower specimens, respectively, as well as large parts of the mitochondrial genome of the Forbes' Quarry individual. We confirm that the Forbes' Quarry individual was a female and the Devil's Tower individual a male. We also show that the Forbes' Quarry individual is genetically more similar to the ∼120,000-y-old Neanderthals from Scladina Cave in Belgium (Scladina I-4A) and Hohlenstein-Stadel Cave in Germany, as well as to a ∼60,000- to 70,000-y-old Neanderthal from Russia (Mezmaiskaya 1), than to a ∼49,000-y-old Neanderthal from El Sidrón (El Sidrón 1253) in northern Spain and other younger Neanderthals from Europe and western Asia. This suggests that the Forbes' Quarry fossil predates the latter Neanderthals. The preservation of archaic human DNA in the warm coastal climate of Gibraltar, close to the shores of Africa, raises hopes for the future recovery of archaic human DNA from regions in which climatic conditions are less than optimal for DNA preservation.

Keywords: Forbes’ Quarry; Gibraltar Neanderthal; ancient DNA; library preparation; paleogenetics.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
(A) Geographic locations of Gibraltar and other sites that are discussed in this study. (B) The Forbes’ Quarry cranium (Top) and the cranium and mandible of an infant found at Devil’s Tower (Bottom) on Gibraltar. Reprinted with permission from ref. .
Fig. 2.
Fig. 2.
Frequencies of C-to-T substitutions at the ends of sequence alignments for the Forbes’ Quarry and Devil’s Tower individuals. Only sequences of length ≥35 bp were used in this analysis. Conditional substitution frequencies were computed by filtering for sequences that carry a C-to-T substitution on the opposing end.
Fig. 3.
Fig. 3.
(A) Maximum-likelihood tree of the mitochondrial DNA sequences from Forbes’ Quarry, 25 modern humans (collapsed), 23 Neanderthals, 4 Denisovans, and the Sima de los Huesos individual (see SI Appendix, Table S4 for a complete list of mitochondrial genomes and accession numbers). The chimpanzee mitochondrial genome was used as an outgroup (not shown). Support from 100 bootstrap replicates is shown next to the nodes. (B) Derived allele sharing with human (Mbuti), Neanderthal (Altai), and the Denisovan (Denisova 3) for sequences of Forbes’ Quarry and Devil’s Tower showing signs of deamination. 95% binomial confidence intervals are shown in parentheses.
Fig. 4.
Fig. 4.
(A) D-statistics of low-coverage Neanderthals compared with high-quality genomes of Vindija 33.19, Chagyrskaya 8, and the Altai Neanderthal. Bars indicate 1 SD, as obtained by weighted-block jackknife. Green bars indicate that D is significantly (Z ≥ 3) different from zero. Only transversions were considered to suppress the influence of deamination-induced substitutions. (B) Population split times inferred by F(A|B) statistics. Blue circles indicate ages of the Neanderthal individuals estimated from branch shortening, black circles denote population split times from Vindija 33.19, and black lines correspond to 95% confidence intervals. Scl I-4A, Scladina I-4A; Mez1, Mezmaiskaya 1; Mez2, Mezmaiskaya 2; HST, Hohlenstein-Stadel.

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