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The genomic natural history of the aurochs

Naturevolume 635, pages136–141 (2024)Cite this article

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Abstract

Now extinct, the aurochs (Bos primigenius) was a keystone species in prehistoric Eurasian and North African ecosystems, and the progenitor of cattle (Bos taurus), domesticates that have provided people with food and labour for millennia1. Here we analysed 38 ancient genomes and found 4 distinct population ancestries in the aurochs—European, Southwest Asian, North Asian and South Asian—each of which has dynamic trajectories that have responded to changes in climate and human influence. Similarly toHomo heidelbergensis, aurochsen first entered Europe around 650 thousand years ago2, but early populations left only trace ancestry, with both North Asian and EuropeanB. primigenius genomes coalescing during the most recent glaciation. North Asian and European populations then appear separated until mixing after the climate amelioration of the early Holocene. European aurochsen endured the more severe bottleneck during the Last Glacial Maximum, retreating to southern refugia before recolonizing from Iberia. Domestication involved the capture of a small number of individuals from the Southwest Asian aurochs population, followed by early and pervasive male-mediated admixture involving each ancestral strain of aurochs after domestic stocks dispersed beyond their cradle of origin.

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Fig. 1: Temporal, geographical and genetic location of 72 ancientBos genomes.
Fig. 2: Plots of ancestral components in aurochs and domestic cattle genomes.
Fig. 3: Phylogenies of whole genomes and mtDNA.
Fig. 4: Estimation of the past demography of the aurochs.

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Data availability

Sequence reads and alignment files of new data are available through the ENA under accession numberPRJEB75467. Previously published ancient data used in this study are available under accession numbersPRJEB31621,PRJNA379859,PRJNA803479 andPRJEB74338, and are detailed in Supplementary Table2. Sources for previously published modern genomic data analysed here are listed in Supplementary Table3. The ARS-UCD1.2 reference genome is available under NCBI assembly accessionGCF_002263795.1. TheB. taurus mitochondrial reference genome is available under NCBI accession numberV00654.1.

Code availability

This study makes use of publicly available software, referenced throughout the main text and supplementary material.

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Acknowledgements

This work is funded by the European Research Council under the European Union’s Horizon 2020 research and innovation program, grant agreements 885729-AncestralWeave and 295729-CodeX. M.-H.S.S. is supported by the Carlsberg Foundation (Reintegration Fellowship, CF20-0355) and the Independent Research Fund Denmark (International Postdoc, 8020-00005B), which also contributed to the sequencing costs and carbon dating costs of this project; E.R. is supported by the Jan Löfqvist Endowment and Axel and Margaret Ax:son Johnson Foundation for Public Benefit and contributed to the sequencing and carbon dating costs of this project; K.G.D. is supported by Science Foundation Ireland (grant number 21/PATH-S/9515/); V.E.M. is supported by a Government of Ireland Postdoctoral Fellowship (GOIPD/2020/605); A.G.-d. and A.V.-G. are supported by Xunta de Galicia (CN 2021/17); M. Sablin is supported by state assignment no. 122031100282-2; A.A.T. is supported by the Russian Science Foundation (‘The World of Ancient Nomads of Inner Asia: Interdisciplinary Studies of Material Culture, Sculptures and Economy’, project no. 22-18-00470); and C.A.M. is supported by the European Council for Research for a Horizon 2020 grant (ASIAPAST, action no. 772957). We thank TrinSeq for sequencing support; L. Cassidy and L. Wright for discussions; R. Verdugo for contributions to figure design; the Margulan Institute of Archaeology Committee of the Ministry of Science and Higher Education of the Republic of Kazakhstan for storing, archiving and providing the material from the Roschinskoe site; the Museum of the Institute of Plant and Animal Ecology (Ural Branch of the Russian Academy of Sciences, Ekaterinburg) for providing specimens for sampling; A. Zeeb-Lanz and R. Arbogast for permitting the sampling of bones from Herxheim; R. W. Schmitz for permitting the sampling of bones from Bedburg-Königshoven; and H. Hartnagel for assistance in sampling the Rhine specimens.

Author information

Author notes

  1. Deceased: Viktor Zeibert

Authors and Affiliations

  1. Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland

    Conor Rossi, Victoria E. Mullin, Amelie Scheu, Jolijn A. M. Erven, Marta Pereira Verdugo, Kevin G. Daly, Valeria Mattiangeli, Matthew D. Teasdale, Deborah Diquelou & Daniel G. Bradley

  2. Department of Biology, University of Copenhagen, Copenhagen, Denmark

    Mikkel-Holger S. Sinding

  3. Palaeogenetics Group, Institute of Organismic and Molecular Evolution (iomE), Johannes Gutenberg University Mainz, Mainz, Germany

    Amelie Scheu & Joachim Burger

  4. Groningen Institute of Archaeology, University of Groningen, Groningen, The Netherlands

    Jolijn A. M. Erven

  5. School of Agriculture and Food Science, University College Dublin, Dublin, Ireland

    Kevin G. Daly

  6. Globe Institute, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Marta Maria Ciucani, Pernille Bangsgaard, Matthew Collins & M. Thomas P. Gilbert

  7. Bioinformatics Support Unit, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, UK

    Matthew D. Teasdale

  8. Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK

    Aurélie Manin, Ashleigh F. Haruda, Kristina Tabbada & Greger Larson

  9. McDonald Institute for Archaeological Research, University of Cambridge, Cambridge, UK

    Matthew Collins

  10. Independent researcher, Langcliffe, UK

    Tom C. Lord

  11. Institute of Archaeology and Steppe Civilizations, Al-Farabi Kazakh National University, Almaty, Kazakhstan

    Viktor Zeibert

  12. Sezione di Geologia e Paleontologia, Museo Civico di Storia Naturale di Verona, Verona, Italy

    Roberto Zorzin

  13. Vendsyssel Historical Museum, Hjørring, Denmark

    Michael Vinter

  14. Department of Natural Sciences, National Museums Scotland, Edinburgh, UK

    Zena Timmons & Andrew C. Kitchener

  15. School of Geosciences, University of Edinburgh, Edinburgh, UK

    Andrew C. Kitchener

  16. LEIZA, Archaeological Research Centre and Museum for Human Behavioural Evolution, Schloss Monrepos, Neuwied, Germany

    Martin Street

  17. Palaeogenomics Group, Institute of Palaeoanatomy, Domestication Research and the History of Veterinary Medicine, Ludwig-Maximilians-Universität, Munich, Germany

    Laurent A. F. Frantz

  18. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Laurent A. F. Frantz

  19. Institute for Prehistory and Protohistory, University of Cologne, Cologne, Germany

    Birgit Gehlen

  20. Bioarchaeology Service, Museo delle Civiltà, Piazza Guglielmo Marconi, Rome, Italy

    Francesca Alhaique & Antonio Tagliacozzo

  21. Sezione di Geologia e Paleontologia, Museo della Natura e dell’ Uomo, Padova, Italy

    Mariagabriella Fornasiero

  22. Dipartimento di Scienze della Terra, Università di Pisa, Pisa, Italy

    Luca Pandolfi

  23. Department of Paleontology and Mineralogy, National Museum of Natural History, Bulgarian Academy of Sciences, Sofia, Bulgaria

    Nadezhda Karastoyanova

  24. National Museum of Denmark, Copenhagen, Denmark

    Lasse Sørensen

  25. Department of Recreational Geography, Service, Tourism and Hospitality, Institute of Geography, Altai State University, Barnaul, Russian Federation

    Kirill Kiryushin

  26. The Biological Museum, Lund University, Arkivcentrum Syd, Lund, Sweden

    Jonas Ekström & Maria Mostadius

  27. Instituto Universitario de Xeoloxía, Universidade da Coruña (UDC), A Coruña, Spain

    Aurora Grandal-d’Anglade & Amalia Vidal-Gorosquieta

  28. German Archaeological Institute, Central Department, Berlin, Germany

    Norbert Benecke

  29. Lauresham Laboratory for Experimental Archaeology, UNESCO-Welterbestätte Kloster Lorsch, Lorsch, Germany

    Claus Kropp

  30. Department of Archaeology, Ethnography and Museology, Altai State University, Barnaul, Russian Federation

    Sergei P. Grushin & Alexey A. Tishkin

  31. Toraighyrov University, Joint Research Center for Archeological Studies, Pavlodar, Kazakhstan

    Ilja Merts & Viktor Merts

  32. Department of Archaeology and History, University of Exeter, Exeter, UK

    Alan K. Outram

  33. Department of Archaeology and Ancient History, Lund University, Lund, Sweden

    Erika Rosengren

  34. Centre for Palaeogenetics, Stockholm, Sweden

    Erika Rosengren

  35. Lund University Historical Museum, Lund, Sweden

    Erika Rosengren

  36. Paleoecology Laboratory, Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences, Ekaterinburg, Russian Federation

    Pavel Kosintsev

  37. Department of History, Institute of Humanities, Ural Federal University, Ekaterinburg, Russian Federation

    Pavel Kosintsev

  38. Zoological Institute of the Russian Academy of Sciences, Saint Petersburg, Russian Federation

    Mikhail Sablin

  39. Archaeology Stable Isotope Laboratory, Institute of Pre- and Protohistoric Archaeology, University of Kiel, Kiel, Germany

    Cheryl A. Makarewicz

  40. University of Haifa, Haifa, Israel

    Cheryl A. Makarewicz

Authors
  1. Conor Rossi

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  2. Mikkel-Holger S. Sinding

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  3. Victoria E. Mullin

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  4. Amelie Scheu

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  5. Jolijn A. M. Erven

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  6. Marta Pereira Verdugo

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  7. Kevin G. Daly

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  8. Marta Maria Ciucani

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  9. Valeria Mattiangeli

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  10. Matthew D. Teasdale

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  11. Deborah Diquelou

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  12. Aurélie Manin

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  13. Pernille Bangsgaard

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  14. Matthew Collins

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  15. Tom C. Lord

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  16. Viktor Zeibert

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  17. Roberto Zorzin

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  18. Michael Vinter

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  19. Zena Timmons

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  20. Andrew C. Kitchener

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  21. Martin Street

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  22. Ashleigh F. Haruda

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  23. Kristina Tabbada

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  24. Greger Larson

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  25. Laurent A. F. Frantz

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  26. Birgit Gehlen

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  27. Francesca Alhaique

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  28. Antonio Tagliacozzo

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  29. Mariagabriella Fornasiero

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  30. Luca Pandolfi

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  31. Nadezhda Karastoyanova

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  32. Lasse Sørensen

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  33. Kirill Kiryushin

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  34. Jonas Ekström

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  35. Maria Mostadius

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  36. Aurora Grandal-d’Anglade

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  37. Amalia Vidal-Gorosquieta

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  38. Norbert Benecke

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  39. Claus Kropp

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  40. Sergei P. Grushin

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  41. M. Thomas P. Gilbert

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  42. Ilja Merts

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  43. Viktor Merts

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  44. Alan K. Outram

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  45. Erika Rosengren

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  46. Pavel Kosintsev

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  47. Mikhail Sablin

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  48. Alexey A. Tishkin

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  49. Cheryl A. Makarewicz

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  50. Joachim Burger

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  51. Daniel G. Bradley

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Contributions

D.G.B. and M.-H.S.S. conceived the project. Laboratory work was done by C.R., M.-H.S.S., V.E.M., A.S., M.P.V., K.G.D., M.M.C., V.M., D.D. A.M. and P.B. C.R. processed and analysed the data with contributions from M.-H.S.S., V.E.M., J.A.M.E. and K.G.D. All other authors gave access to samples, provided archaeological and osteological context and aided in the interpretation of results. The manuscript was written by D.G.B., C.R., M,-H.S.S. and V.E.M., with contributions from all co-authors.

Corresponding authors

Correspondence toMikkel-Holger S. Sinding orDaniel G. Bradley.

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Competing interests

The authors declare no competing interests.

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Nature thanks the anonymous reviewer(s) for their contribution to the peer review of this work.Peer reviewer reports are available.

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Extended data figures and tables

Extended Data Fig. 1 Three genomic groups within European aurochs.

a, Heat map of pairwise IBS distance values between European aurochsen drawn using pheatmap (https://github.com/raivokolde/pheatmap). European aurochs cluster into geographically coherent groups; western Europe, Italy and the Balkans. Genomes from Iberia cluster within the western European group, consistent with the Iberian glacial refugium being a source of postglacial recolonization. The lowest pairwise IBS distances are observed in a tight Scandinavian cluster of five genomes in the top left corner.b, Best-fitting model estimated using AdmixtureGraph allowingm = 2 admixture edges. This infers a closely shared evolutionary history among western European genomes (Iberia, Britain, Germany, Scandinavia). Italians derive from a more basal European source but also have ~12% admixture contribution of a Southwest Asian population. Balkans genomes are modelled as having ~41% Southwest Asian contribution.

Extended Data Fig. 2 MSMC2 cross-population analysis.

MSMC2 was used to perform cross-population analysis to determine the approximate divergence time between four putative postglacial Eurasian populations; European aurochsen, North Asian aurochsen, Southwest Asian aurochsen (represented by the Anatolian Neolithic, Sub1), South AsianBos namadicus (represented by their descendants, South Asian indicine). The relative cross-coalescence rate (CCR) was computed between all population pairings of the four populations of aurochs and the split time between two populations was estimated as the time interval at the relative CCR of 0.5. Three splits were observed; first European aurochs versus Near Eastern aurochs during the LGM, second European and Southwest Asian/Near Eastern aurochs versus north Asian aurochs during MIS 5, third allBos primigenius populations versusBos indicus (proxy forBos namadicus). The timings of these splits reflect the phylogenetic relationship of the populations.

Extended Data Fig. 3 Summary of analyses timing the divergence of Southwest Asian and European aurochs populations versus North Asian aurochs populations.

The top panel displays the range of estimates observed when X chromosome divergence began based on pseudodiploid X chromosome analysis of 10 pairs of North Asian-Southwest Asian/European samples (Supplementary Information Section 4). The second panel displays the range of split time between Southwest Asian/European aurochsen and North Asian aurochsen estimated by MSMC2 cross-population analysis (Extended Data Fig.2). The third panel displays the 95% HPD interval of major mtDNA haplogroup divergences associated with Southwest Asian/European aurochsen and North Asian aurochsen splits. The final panel displays the LR04 stack of benthic d18O records89 overlaid with MIS periods21. Interglacial periods (MIS 1, MIS 5e) are coloured red, stadial periods (MIS 2-4, MIS 5b, MIS 5d) are coloured blue and interstadial periods (MIS 5a and 5c) are coloured yellow. All divergence estimates overlap with the final interstadial of MIS 5.

Extended Data Fig. 4 NGSadmixK = 4 composition, mitochondrial haplogroups and14C dates of 16 HoloceneBos sampled from Asia.

Pleistocene North Asian samples (Tula1, Baikal1, Gyu1) display an unadmixed ancestral profile that stretches from ~41.5 to ~12.2 ka. By contrast, Holocene Asian aurochsen display an admixed ancestral profile and four separate wild maternal lineages, including the EuropeanP haplogroup and the Southwest AsianQ. The advent of Central Asian domestic taurine cattle during the Bronze Age presents a different ancestral profile, where animals are modelled mostly with the Southwest Asian ancestral component typical ofBos taurus, although also with minor North Asian and Europe wild components reflecting introgression from local wild herds (Supplementary Information Section 6). Domestic maternal haplotypes (T3) are detected in 4 of 5 Central Asian domesticates.

Extended Data Fig. 5 Unequal Bovini allele sharing inBos.

We explicitly tested allele sharing ofBos populations (East Asian indicine,n = 3; South Asian indicine,n = 4; North Asia,n = 3; Rhine,n = 2; North Africa wild,n = 1; Neolithic Anatolia,n = 3; Southwest Asia wild,n = 1). with wild Eurasian Bovini (Banteng,n = 4; Gaur,n = 3; Wild Yak,n = 3; Wisent,n = 1) relative to western European aurochs (n = 12) usingD (water buffalo (n = 3), Bovini sp.; western Europe,Bos test) using SNPs called on Bovini outgroups. We repeatedly observed significant excess allele sharing between indicine and outgroup Bovini species compared to western European populations. All otherBos primigenius/Bos taurus populations suggest clade integrity, except Pleistocene North Asia which displayed slightly higher allele sharing with Bovini outgroups, but at an order of magnitude lower than that shown byBos indicus. Error bars depict the standard error of each test multiplied by 3.

Extended Data Fig. 6 Sex bias in domestic introgression.

We explicitly tested allele sharing ofBos populations with aurochsen (n = 15) relative to Neolithic Anatolian cattle (n = 3) with (D (water buffalo (n = 3), aurochs population; Neolithic Anatolia, test sample) using two pseudohaploid datasets (SNPs called on the autosome and SNPs called on the X chromosome). In domestic samples (n = 21) there is a pattern of increased autosomal contribution relative to the X chromosome, suggesting introgression was male biased. This contrasts with the patterns observed in wild populations, where the minor component is more often female-biased. Error bars depict the standard error of each test multiplied by 3.

Extended Data Fig. 7 Maximum likelihood phylogeny constructed from Y chromosomal sequences of 206 ancient and modernBos samples.

Patterns within the phylogeny reveal thatBos taurus andBos primigenius Y chromosomal variation were not reciprocally monophyletic. Haplotypes of ancient and modern domestic cattle were found in six distinct clades and in one solitary individual, suggesting that there were at least seven male contributions toBos taurus.

Supplementary information

Supplementary Information

Supplementary Information sections 1–6 including Supplementary Figs 1–29, Supplementary Tables 1– 5 and Supplementary References – see contents for details.

Supplementary Data

Supplementary Data 1–6 – see Supplementary Information for full descriptions.

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Rossi, C., Sinding, MH.S., Mullin, V.E.et al. The genomic natural history of the aurochs.Nature635, 136–141 (2024). https://doi.org/10.1038/s41586-024-08112-6

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