Letter | Published:

Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins

Nature 531, 504–507 (24 March 2016) | Download Citation

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Abstract

A unique assemblage of 28 hominin individuals, found in Sima de los Huesos in the Sierra de Atapuerca in Spain, has recently been dated to approximately 430,000 years ago1. An interesting question is how these Middle Pleistocene hominins were related to those who lived in the Late Pleistocene epoch, in particular to Neanderthals in western Eurasia and to Denisovans, a sister group of Neanderthals so far known only from southern Siberia. While the Sima de los Huesos hominins share some derived morphological features with Neanderthals, the mitochondrial genome retrieved from one individual from Sima de los Huesos is more closely related to the mitochondrial DNA of Denisovans than to that of Neanderthals2. However, since the mitochondrial DNA does not reveal the full picture of relationships among populations, we have investigated DNA preservation in several individuals found at Sima de los Huesos. Here we recover nuclear DNA sequences from two specimens, which show that the Sima de los Huesos hominins were related to Neanderthals rather than to Denisovans, indicating that the population divergence between Neanderthals and Denisovans predates 430,000 years ago. A mitochondrial DNA recovered from one of the specimens shares the previously described relationship to Denisovan mitochondrial DNAs, suggesting, among other possibilities, that the mitochondrial DNA gene pool of Neanderthals turned over later in their history.

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Accessions

Primary accessions

European Nucleotide Archive

Data deposits

Sequences generated in this study have been deposited in the European Nucleotide Archive under study accession number PRJEB10597.

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Acknowledgements

We thank B. Höber and A. Weihmann for help with sequencing the libraries, G. Renaud for processing the raw sequence data, S. Castellano and U. Stenzel for discussions and comments on the manuscript. Genetics work was funded by the Max Planck Society and its Presidential Innovation Fund. Field work at the Sierra de Atapuerca sites was funded by the Junta de Castilla y Leon, the Fundacion Atapuerca, the Spanish Ministerio de Ciencia e Innovacion (project CGL2009-12703-C03) and the Spanish Ministerio de Economia y Competitividad (project CGL2012-38434-C03).

Author information

Affiliations

  1. Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany

    • Matthias Meyer
    • , Cesare de Filippo
    • , Sarah Nagel
    • , Ayinuer Aximu-Petri
    • , Birgit Nickel
    • , Janet Kelso
    • , Kay Prüfer
    •  & Svante Pääbo

  2. Centro de Investigación Sobre la Evolución y Comportamiento Humanos, Universidad Complutense de Madrid–Instituto de Salud Carlos III, 28029 Madrid, Spain

    • Juan-Luis Arsuaga
    • , Ignacio Martínez
    •  & Ana Gracia

  3. Departamento de Paleontología, Facultad de Ciencias Geológicas, Universidad Complutense de Madrid, 28040 Madrid, Spain

    • Juan-Luis Arsuaga

  4. Área de Paleontología, Departamento de Geografía y Geología, Universidad de Alcalá, Alcalá de Henares, 28871 Madrid, Spain

    • Ignacio Martínez
    •  & Ana Gracia

  5. Centro Nacional de Investigación sobre la Evolución Humana, Paseo Sierra de Atapuerca, 09002 Burgos, Spain

    • José María Bermúdez de Castro

  6. Department of Anthropology, University College London, 14 Taviton Street, London WC1H 0BW, UK

  7. Institut Català de Paleoecologia Humana i Evolució Social, C/Marcel·lí Domingo s/n (Edifici W3), Campus Sescelades, 43007 Tarragona, Spain

    • Eudald Carbonell

  8. Àrea de Prehistòria, Departament d’Història i Història de l’Art, Universitat Rovira i Virgili, Facultat de Lletres, Avinguda de Catalunya, 35, 43002 Tarragona, Spain

    • Eudald Carbonell

  9. Department of Anthropology, University of Toronto, 19 Russell Street, Toronto, Ontario M5S 2S2, Canada

    • Bence Viola

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Contributions

M.M., J.-L.A. and S.P. directed the experimental work and wrote the manuscript. M.M. designed the laboratory experiments, which S.N., A.A. and B.N. performed. M.M., C.d.F., B.V., J.K. and K.P. analysed the data. J.-L.A., I.M., A.G., J.M.B. and E.C. excavated the fossil and provided archaeological expertise.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Matthias Meyer.

Extended data

Extended data figures

  1. 1.

    Sharing of derived alleles at diagnostic positions separating the hominin groups in the mitochondrial tree.

  2. 2.

    Frequency of C to T substitutions at the beginning and end of nuclear sequence alignments.

  3. 3.

    Sex determination based on the number of sequences aligning to chromosome X and the autosomes.

  4. 4.

    Number of informative positions identified for each branch of the tree.

  5. 5.

    Derived allele sharing with the Neanderthal- and Denisovan-specific branches in deaminated DNA fragments from all five specimens from SH.

Extended data tables

  1. 1.

    Overview of DNA extracts, libraries and shotgun sequences generated in three experiments

  2. 2.

    Characteristics of sequences obtained after mtDNA enrichment

  3. 3.

    Fraction of derived alleles shared with the human, Neanderthal and Denisovan genomes and combinations thereof

  4. 4.

    Derived allele sharing between putatively deaminated DNA fragments of the five SH specimens and all branches of the hominin evolutionary tree

  5. 5.

    Overview of the sequencing runs performed

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text, Supplementary Figures 1-2, Supplementary Tables 1-4 and additional references.

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DOI

https://doi.org/10.1038/nature17405

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