The population dynamics of the Pleistocene woolly mammoth (Mammuthus primigenius) has been the subject of intensive palaeogenetic research. Although a large number of mitochondrial genomes across Eurasia have been reconstructed, the available data remains geographically sparse and mostly focused on eastern Eurasia. Thus, population dynamics in other regions have not been extensively investigated. Here, we use a multi-method approach utilising proteomic, stable isotope and genetic techniques to identify and generate twenty woolly mammoth mitochondrial genomes, and associated dietary stable isotopic data, from highly fragmentary Late Pleistocene material from central Europe. We begin to address region-specific questions regarding central European woolly mammoth populations, highlighting parallels with a previous replacement event in eastern Eurasia ten thousand years earlier. A high number of shared derived mutations between woolly mammoth mitochondrial clades are identified, questioning previous phylogenetic analysis and thus emphasizing the need for nuclear DNA studies to explicate the increasingly complex genetic history of the woolly mammoth.

Centre for Cultural Anthropology Moravian Museum Zelný trh 6 65937 Brno Czech Republic

Département de Préhistoire du MNHN Institut de Paléontologie Humaine 1 rue René Panhard 75 013 Paris France

Department of Anthropology Faculty of Philosophy and Arts University of West Bohemia Sedláčkova 15 306 14 Pilsen Czech Republic

Department of Archaeogenetics Max Planck Institute for the Science of Human History Kahlaische Straße 10 07745 Jena Germany

Department of Early Prehistory and Quaternary Ecology Schloss Hohentubingen 72070 Tübingen Germany

Department of Geosciences University of Tübingen Hölderlinstraße 12 72074 Tübingen Germany

Department of Human Evolution Max Planck Institute for Evolutionary Anthropology Deutscher Pl 6 04103 Leipzig Germany

Hrdlicka Museum of Man Faculty of Science CU Viničná 7 128 00 Praha Czech Republic

Institute for Archaeological Science University of Tübingen Rümelinstraße 23 72070 Tübingen Germany

Quantitative Biology Centre Tubingen University of Tübingen Auf der Morgenstelle 10 72076 Tübingen Germany

Senckenberg Centre for Human Evolution and Paleoenvironment University of Tübingen Hölderlinstraße 12 72074 Tübingen Germany

The Institute of Systematics and Evolution of Animals Polish Academy of Sciences Sławkowska 17 31 016 Kraków Poland

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Barnes I, et al. Genetic structure and extinction of the woolly mammoth. Mammuthus primigenius. Current Biology. 2007;17:1072–1075. doi: 10.1016/j.cub.2007.05.035. PubMed DOI

Palkopoulou E, et al. Holarctic genetic structure and range dynamics in the woolly mammoth. Proceedings of the Royal Society B: Biological Sciences. 2013;280:20131910. doi: 10.1098/rspb.2013.1910. PubMed DOI PMC

Chang D, et al. The evolutionary and phylogeographic history of woolly mammoths: a comprehensive mitogenomic analysis. Sci. Rep. 2017;7:44585. doi: 10.1038/srep44585. PubMed DOI PMC

Enk, J.

Gilbert MTP, et al. Intraspecific phylogenetic analysis of Siberian woolly mammoths using complete mitochondrial genomes. Proc. Natl. Acad. Sci. USA. 2008;105:8327–8332. doi: 10.1073/pnas.0802315105. PubMed DOI PMC

Debruyne R, et al. Out of America: ancient DNA evidence for a new world origin of late quaternary woolly mammoths. Current Biology. 2008;18:1320–1326. doi: 10.1016/j.cub.2008.07.061. PubMed DOI

Drucker DG, et al. Tracking possible decline of woolly mammoth during the Gravettian in Dordogne (France) and the Ach valley (Germany) using multi-isotope tracking (13C, 14C, 15N, 34S, 18O) Quat. Int. 2015;359–360:304–317. doi: 10.1016/j.quaint.2014.11.028. DOI

Bocherens H. Isotopic biogeochemistry and the palaeoecology of the mammoth steppe fauna. Deinsea. 2003;9:57–76.

Schwartz-Narbonne R, Longstaffe FJ, Metcalfe JZ, Zazula G. Solving the woolly mammoth conundrum: amino acid 15N-enrichment suggests a distinct forage or habitat. Sci. Rep. 2015;5:9791. doi: 10.1038/srep09791. PubMed DOI PMC

Higham T, et al. Testing models for the beginnings of the Aurignacian and the advent of figurative art and music: the radiocarbon chronology of Geißenklösterle. J. Hum. Evol. 2012;62:664–676. doi: 10.1016/j.jhevol.2012.03.003. PubMed DOI

Drucker, D. G., Rivals, F., Münzel, S. C. & Bocherens, H. Stable isotope and microwear investigation on the mammoth (

Bocherens H, et al. Reconstruction of the Gravettian food-web at Pȓedmost I using multi-isotopic tracking (13c, 15N, 34S) of bone collagen. Quat. Int. 2015;359–360:211–228. doi: 10.1016/j.quaint.2014.09.044. DOI

Münzel SC, Wolf S, Drucker DG, Conard NJ. The exploitation of mammoth in the Swabian Jura (SW-Germany) during the aurignacian and gravettian period. Quat. Int. 2017;445:184–199. doi: 10.1016/j.quaint.2016.08.013. DOI

DeNiro MJ. Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature. 1985;317:806–809. doi: 10.1038/317806a0. DOI

DeNiro MJ, Weiner S. Chemical, enzymatic and spectroscopic characterization of “collagen” and other organic fractions from prehistoric bones. Geochim. Cosmochim. Acta. 1988;52:2197–2206. doi: 10.1016/0016-7037(88)90122-6. DOI

Ambrose SH. Preparation and characterization of bone and tooth collagen for isotopic analysis. J. Archaeol. Sci. 1990;17:431–451. doi: 10.1016/0305-4403(90)90007-R. DOI

Münzel, S. C. The production of Upper Palaeolithic mammoth bone artifacts from southwestern Germany. In Caverretta, G., Gioia, P., Muss, M. & Palombo, M. R. (eds)

Münzel, S. C. Mammoth remains in the Upper and Middle Paleolithic layers of Geißenklösterle cave (Ach valley, Swabian Jura, southwestern Germany): Hunting season, acquisition of raw material and tool production at Geißenklösterle cave. In Vialou, D., Renault-MIskovsky, J. & Patou-Mathis, M. (eds)

Prendergast ME, et al. Reconstructing asian faunal introductions to eastern africa from multi-proxy biomolecular and archaeological datasets. PloS one. 2017;12:e0182565. doi: 10.1371/journal.pone.0182565. PubMed DOI PMC

Welker F, et al. Palaeoproteomic evidence identifies archaic hominins associated with the Châtelperronian at the Grotte du Renne. Proc. Natl. Acad. Sci. USA. 2016;113:11162–11167. doi: 10.1073/pnas.1605834113. PubMed DOI PMC

Münzel, S. C. Subsistence patterns in the Gravettian of the Ach valley, a former tributary of the Danube in the Swabian Jura. In Svoboda, J. A. & Sedláčková, L. (eds)

Conard, N. J., Kitagawa, K., Krönneck, P., Böhme, M. & Münzel, S. C. The importance of fish, fowl and small mammals in the Paleolithic diet of the Swabian Jura, southwestern Germany. In

Sawyer S, Krause J, Guschanski K, Savolainen V, Pääbo S. Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS One. 2012;7:e34131. doi: 10.1371/journal.pone.0034131. PubMed DOI PMC

Bollongino R, Tresset A, Vigne J-D. Environment and excavation: Pre-lab impacts on ancient DNA analyses. C. R. Palevol. 2008;7:91–98. doi: 10.1016/j.crpv.2008.02.002. DOI

Gilbert MTP, et al. Whole-genome shotgun sequencing of mitochondria from ancient hair shafts. Science. 2007;317:1927–1930. doi: 10.1126/science.1146971. PubMed DOI

Krause J, et al. Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae. Nature. 2006;439:724–727. doi: 10.1038/nature04432. PubMed DOI

Rogaev EI, et al. Complete mitochondrial genome and phylogeny of Pleistocene mammoth Mammuthus primigenius. PLoS Biol. 2006;4:e73. doi: 10.1371/journal.pbio.0040073. PubMed DOI PMC

Poinar HN, et al. Metagenomics to paleogenomics: large-scale sequencing of mammoth DNA. Science. 2006;311:392–394. doi: 10.1126/science.1123360. PubMed DOI

Maricic T, Whitten M, Pääbo S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS One. 2010;5:e14004. doi: 10.1371/journal.pone.0014004. PubMed DOI PMC

Talamo S, et al. Direct radiocarbon dating and genetic analyses on the purported neanderthal mandible from the Monti Lessini (Italy) Sci. Rep. 2016;6:29144. doi: 10.1038/srep29144. PubMed DOI PMC

Charlton, S.

Piganeau G, Eyre-Walker A. A reanalysis of the indirect evidence for recombination in human mitochondrial DNA. Heredity. 2004;92:282–288. doi: 10.1038/sj.hdy.6800413. PubMed DOI

Ballard JWO, Whitlock MC. The incomplete natural history of mitochondria. Mol. Ecol. 2004;13:729–744. doi: 10.1046/j.1365-294X.2003.02063.x. PubMed DOI

Rieux, A. & Balloux, F. Inferences from tip-calibrated phylogenies: a review and a practical guide. PubMed PMC

Lorenzen ED, et al. Species-specific responses of Late Quaternary megafauna to climate and humans. Nature. 2011;479:359–364. doi: 10.1038/nature10574. PubMed DOI PMC

Puzachenko, A. Y.

Bocherens H, Drucker D, Billiou D, Moussa I. Une nouvelle approche pour évaluer l'état de conservation de l’os et du collagène pour les mesures isotopiques (datation au radiocarbone, isotopes stables du carbone et de l’azote) Anthropologie. 2005;109:557–567. doi: 10.1016/j.anthro.2005.06.005. DOI

Longin R. New method of collagen extraction for radiocarbon dating. Nature. 1971;230:241–242. doi: 10.1038/230241a0. PubMed DOI

Bocherens H, et al. Paleobiological implications of the isotopic signatures (13C, 15N) of fossil mammal collagen in Scladina Cave (Sclayn, Belgium) Quat. Res. 1997;48:370–380. doi: 10.1006/qres.1997.1927. DOI

Buckley M, Collins M, Thomas-Oates J, Wilson JC. Species identification by analysis of bone collagen using matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 2009;23:3843–3854. doi: 10.1002/rcm.4316. PubMed DOI

Welker F, Soressi M, Rendu W, Hublin J-J, Collins MJ. Using ZooMS to identify fragmentary bone from the late Middle/Early Upper Palaeolithic sequence of Les Cottés, France. J. Archaeol. Sci. 2015;54:279–286. doi: 10.1016/j.jas.2014.12.010. DOI

Welker F, et al. Ancient proteins resolve the evolutionary history of Darwin’s South American ungulates. Nature. 2015;522:81–84. doi: 10.1038/nature14249. PubMed DOI

Buckley M, Larkin N, Collins M. Mammoth and mastodon collagen sequences; survival and utility. Geochim. Cosmochim. Acta. 2011;75:2007–2016. doi: 10.1016/j.gca.2011.01.022. DOI

Pääbo S, et al. Genetic analyses from ancient DNA. Annu. Rev. Genet. 2004;38:645–679. doi: 10.1146/annurev.genet.37.110801.143214. PubMed DOI

Dabney J, et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. USA. 2013;110:15758–15763. doi: 10.1073/pnas.1314445110. PubMed DOI PMC

Meyer M, Kircher M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. 2010;2010:db.prot5448. doi: 10.1101/pdb.prot5448. PubMed DOI

Kircher M, Sawyer S, Meyer M. Double indexing overcomes inaccuracies in multiplex sequencing on the illumina platform. Nucleic Acids Res. 2012;40:e3. doi: 10.1093/nar/gkr771. PubMed DOI PMC

Peltzer A, et al. EAGER: efficient ancient genome reconstruction. Genome Biol. 2016;17:1–14. doi: 10.1186/s13059-016-0918-z. PubMed DOI PMC

Briggs AW, et al. Patterns of damage in genomic DNA sequences from a neandertal. Proc. Natl. Acad. Sci. USA. 2007;104:14616–14621. doi: 10.1073/pnas.0704665104. PubMed DOI PMC

Parks M, Lambert D. Impacts of low coverage depths and post-mortem DNA damage on variant calling: a simulation study. BMC Genomics. 2015;16:19. doi: 10.1186/s12864-015-1219-8. PubMed DOI PMC

Enk J, et al. Complete Columbian mammoth mitogenome suggests interbreeding with woolly mammoths. Genome Biol. 2011;12:R51. doi: 10.1186/gb-2011-12-5-r51. PubMed DOI PMC

Kearse M, et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC

Keane TM, Creevey CJ, Pentony MM, Naughton TJ, Mclnerney JO. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol. Biol. 2006;6:29. doi: 10.1186/1471-2148-6-29. PubMed DOI PMC

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods. 2012;9:772. doi: 10.1038/nmeth.2109. PubMed DOI PMC

Chernomor, O., von Haeseler, A. & Minh, B. Q. Terrace aware data structure for phylogenomic inference from supermatrices. PubMed PMC

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Minh BQ, Nguyen MAT, von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 2013;30:1188–1195. doi: 10.1093/molbev/mst024. PubMed DOI PMC

Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Ronquist F, et al. MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

R Core Team.

Wickham, H.

Ramsey CB. Bayesian analysis of radiocarbon dates. Radiocarbon. 2009;51:337–360. doi: 10.1017/S0033822200033865. DOI

Reimer PJ, et al. IntCal13 and marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon. 2013;55:1869–1887. doi: 10.2458/azu_js_rc.55.16947. DOI

Ancient DNA of narrow-headed vole reveal common features of the Late Pleistocene population dynamics in cold-adapted small mammals