Abstract
In studying the genomes of extinct species, two principal limitations are typically the small quantities of endogenous ancient DNA and its degraded condition1, even though products of up to 1,600 base pairs (bp) have been amplified in rare cases2. Using small overlapping polymerase chain reaction products, longer stretches of sequences or even whole mitochondrial genomes3,4 can be reconstructed, but this approach is limited by the number of amplifications that can be performed from rare samples. Thus, even from well-studied Pleistocene species such as mammoths, ground sloths and cave bears, no DNA sequences of more than about 1,000 bp have been reconstructed5,6,7. Here we report the complete mitochondrial genome sequence of the Pleistocene woolly mammoth Mammuthus primigenius. We used about 200 mg of bone and a new approach that allows the simultaneous retrieval of multiple sequences from small amounts of degraded DNA. Our phylogenetic analyses show that the mammoth was more closely related to the Asian than to the African elephant. However, the divergence of mammoth, African and Asian elephants occurred over a short time, corresponding to only about 7% of the total length of the phylogenetic tree for the three evolutionary lineages.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Pääbo, S. et al. Genetic analyses from ancient DNA. Annu. Rev. Genet. 38, 645–679 (2004)
Lambert, D. M. et al. Rates of evolution in ancient DNA from Adelie penguins. Science 295, 2270–2273 (2002)
Cooper, A. et al. Complete mitochondrial genome sequences of two extinct moas clarify ratite evolution. Nature 409, 704–707 (2001)
Haddrath, O. & Baker, A. J. Complete mitochondrial DNA genome sequences of extinct birds: ratite phylogenetics and the vicariance biogeography hypothesis. Proc. R. Soc. Lond. B 268, 939–945 (2001)
Höss, M., Dilling, A., Currant, A. & Pääbo, S. Molecular phylogeny of the extinct ground sloth Mylodon darwinii. Proc. Natl Acad. Sci. USA 93, 181–185 (1996)
Loreille, O. et al. Ancient DNA analysis reveals divergence of the cave bear, Ursus spelaeus, and brown bear, Ursus arctos, lineages. Curr. Biol. 11, 200–203 (2001)
Yang, H., Golenberg, E. M. & Shoshani, J. Phylogenetic resolution within the Elephantidae using fossil DNA sequences from the American mastodon (Mammut americanum) as an outgroup. Proc. Natl Acad. Sci. USA 93, 1190–1194 (1996)
Hofreiter, M., Jaenicke, V., Serre, D., von Haeseler, A. & Pääbo, S. DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Res. 29, 4793–4799 (2001)
Bensasson, D., Zhang, D. X., Hartl, D. L. & Hewitt, G. M. Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends Ecol. Evol. 16, 314–321 (2001)
Greenwood, A. D. & Pääbo, S. Nuclear insertion sequences of mitochondrial DNA predominate in hair but not in blood of elephants. Mol. Ecol. 8, 133–137 (1999)
Greenwood, A., Capelli, C., Possnert, G. & Pääbo, S. Nuclear DNA sequences from late Pleistocene megafauna. Mol. Biol. Evol. 16, 1466–1473 (1999)
Noro, M., Masuda, R., Dubrovo, I. A., Yoshida, M. C. & Kato, M. Molecular phylogenetic inference of the woolly mammoth Mammuthus primigenius, based on complete sequences of mitochondrial cytochrome b and 12S ribosomal RNA genes. J. Mol. Evol. 46, 314–326 (1998)
Thomas, M. G., Hagelberg, E., Jone, H. B., Yang, Z. & Lister, A. M. Molecular and morphological evidence on the phylogeny of the Elephantidae. Proc. R. Soc. Lond. B 267, 2493–2500 (2000)
Debruyne, R., Barriel, V. & Tassy, P. Mitochondrial cytochrome b of the Lyakhov mammoth (Proboscidea, Mammalia): new data and phylogenetic analyses of Elephantidae. Mol. Phylogenet. Evol. 26, 421–434 (2003)
Ozawa, T., Hayashi, S. & Mikhelson, V. M. Phylogenetic position of mammoth and Steller's sea cow within Tethytheria demonstrated by mitochondrial DNA sequences. J. Mol. Evol. 44, 406–413 (1997)
Cummings, M. P., Otto, S. P. & Wakeley, J. Sampling properties of DNA sequence data in phylogenetic analysis. Mol. Biol. Evol. 12, 814–822 (1995)
Shoshani, J. Understanding proboscidean evolution: a formidable task. Trends. Ecol. Evol. 13, 480–487 (1998)
Felsenstein, J. Inferring Phylogenies 196–221 (Sinauer Associates, Sunderland, 2004)
Tajima, F. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135, 599–607 (1993)
Felsenstein, J. Confidence-limits on phylogenies with a molecular clock. Syst. Zool. 34, 152–161 (1985)
Tassy, P. in Lothagam: The Dawn of Humanity in Eastern Africa (eds Leakey, M. G. & Harris, J. M.) 331–358 (Columbia Univ. Press, New York, 2003)
Nei, M. in Evolutionary Perspectives and the New Genetics (eds Gershowitz, H., Rucknagel, D. L. & Tashian, R. E.) 133–147 (Alan R. Liss, New York, 1986)
Chen, F. C. & Li, W. H. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am. J. Hum. Genet. 68, 444–456 (2001)
Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460 (1983)
Posada, D. & Crandall, K. A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818 (1998)
Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) (Sinauer Associates, Sunderland, 2003)
Ronquist, F. & Huelsenbeck, J. P. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003)
Schmidt, H. A., Strimmer, K., Vingron, M. & Haeseler, A. TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502–504 (2002)
Hasegawa, M., Kishino, H. & Yano, T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22, 160–174 (1985)
Acknowledgements
We thank the members of our laboratories for discussions and support, G. Khlopatchev for providing the mammoth bone and K. Finstermeier for help with figure design. This work was supported by the Max Planck Society. J.L.P. and M.S. were supported by an NIH grant (to M.S.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The complete mammoth mitochondrial DNA sequence has been deposited in GenBank under accession number DQ188829. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
Supplementary information
Supplementary Methods
Full discription of methods and analysis used in this study. (DOC 142 kb)
Supplementary Table
Table of all primers used in Multiplex PCR. (DOC 149 kb)
Rights and permissions
About this article
Cite this article
Krause, J., Dear, P., Pollack, J. et al. Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae. Nature 439, 724–727 (2006). https://doi.org/10.1038/nature04432
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature04432
This article is cited by
-
Mitochondrial genes as strong molecular markers for species identification
The Nucleus (2023)
-
Genetic diversity and structure of Eurasian otters on Kinmen Island
Conservation Genetics (2023)
-
Distinguishing extant elephants ivory from mammoth ivory using a short sequence of cytochrome b gene
Scientific Reports (2019)
-
Origin and phylogeography of African savannah elephants (Loxodonta africana) in Kruger and nearby parks in southern Africa
Conservation Genetics (2018)
-
Central European Woolly Mammoth Population Dynamics: Insights from Late Pleistocene Mitochondrial Genomes
Scientific Reports (2017)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.