Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Molecular phylogenetics and the origins of placental mammals

Abstract

The precise hierarchy of ancient divergence events that led to the present assemblage of modern placental mammals has been an area of controversy among morphologists, palaeontologists and molecular evolutionists. Here we address the potential weaknesses of limited character and taxon sampling in a comprehensive molecular phylogenetic analysis of 64 species sampled across all extant orders of placental mammals. We examined sequence variation in 18 homologous gene segments (including nearly 10,000 base pairs) that were selected for maximal phylogenetic informativeness in resolving the hierarchy of early mammalian divergence. Phylogenetic analyses identify four primary superordinal clades: (I) Afrotheria (elephants, manatees, hyraxes, tenrecs, aardvark and elephant shrews); (II) Xenarthra (sloths, anteaters and armadillos); (III) Glires (rodents and lagomorphs), as a sister taxon to primates, flying lemurs and tree shrews; and (IV) the remaining orders of placental mammals (cetaceans, artiodactyls, perissodactyls, carnivores, pangolins, bats and core insectivores). Our results provide new insight into the pattern of the early placental mammal radiation.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Phylogenetic relationships among 64 placental mammals and two marsupials based on analysis of 9,779 bp from 15 nuclear and three mtDNA genes.

Similar content being viewed by others

References

  1. Eisenberg, J. F. The Mammalian Radiations (Chicago Univ. Press, Chicago, 1981).

    Google Scholar 

  2. Novacek, M. J. Mammalian phylogeny: shaking the tree. Nature 356, 121–125 (1992).

    Article  ADS  CAS  Google Scholar 

  3. O'Brien, S. J. et al. The promise of comparative genomics in mammals. Science 286, 458–481 (1999).

    Article  CAS  Google Scholar 

  4. Springer, M. S. et al. Endemic African mammals shake the phylogenetic tree. Nature 388, 61–64 (1997).

    Article  CAS  Google Scholar 

  5. Stanhope, M. J. et al. Highly congruent molecular support for a diverse clade of endemic African mammals. Mol. Phylogenet. Evol. 9, 501–508 (1998).

    Article  CAS  Google Scholar 

  6. McKenna, M. C. & Bell, S. K. Classification of Mammals above the Species Level (Columbia Univ. Press, New York, 1997).

    Google Scholar 

  7. Mouchatty, S. K., Gullberg, A., Janke, A. & Arnason, U. The phylogenetic position of the Talpidae within Eutheria based on analysis of complete mitochondrial sequences. Mol. Biol. Evol. 17, 60–67 (2000).

    Article  Google Scholar 

  8. Stanhope, M. J. et al. Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. Proc. Natl Acad. Sci. USA 95, 9967–9972 (1998).

    Article  ADS  CAS  Google Scholar 

  9. Simpson, G. G. The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 85, 1–350 (1945).

    Google Scholar 

  10. McKenna, M. C. in Phylogeny of the Primates: a Multidisciplinary Approach (eds Luckett, W. P. & Szalay, F. S.) 21–46 (Plenum, New York, 1975).

    Book  Google Scholar 

  11. Easteal, S. The pattern of mammalian evolution and the relative rate of molecular evolution. Genetics 124, 165–173 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Kumar, S. & Hedges, S. B. A molecular timescale for vertebrate evolution. Nature 392, 917–920 (1998).

    Article  ADS  CAS  Google Scholar 

  13. Reyes, A. et al. Where do rodents fit? Evidence from the complete mitochondrial genome of Sciurus vulgaris. Mol. Biol. Evol. 17, 979–983 (2000).

    Article  CAS  Google Scholar 

  14. Gregory, W. K. The orders of mammals. Bull. Am. Mus. Nat Hist. 27, 1–524 (1910).

    Google Scholar 

  15. Graur, D., Duret, L. & Gouy, M. Phylogenetic position of the order Lagomorpha (rabbits, hares and allies). Nature 379, 333–335 (1996).

    Article  ADS  CAS  Google Scholar 

  16. Huchon, D., Catzeflis, F. M. & Douzery, E. J. P. Molecular evolution of the nuclear von Willebrand factor gene in mammals and the phylogeny of rodents. Mol. Biol. Evol. 16, 577–589 (1999).

    Article  CAS  Google Scholar 

  17. Kay, R. F., Ross, C. & Williams, B. A. Anthropoid origins. Science 275, 797–804 (1997).

    Article  CAS  Google Scholar 

  18. Pettigrew, J. D. Flying Primates? Megabats have advanced pathway from eye to midbrain. Science 231, 1304–1306 (1986).

    Article  ADS  CAS  Google Scholar 

  19. Waddell, P. J., Okada, N. & Hasegawa, M. Towards resolving the interordinal relationships of placental mammals. Syst. Biol. 48, 1–5 (1999).

    Article  CAS  Google Scholar 

  20. Krettek, A., Gullberg, A. & Arnason, U. Sequence analysis of the complete mitochondrial DNA molecule of the hedgehog, Erinaceus europaeus, and the phylogenetic position of the Lipotyphla. J. Mol. Evol. 41, 952–957 (1995).

    Article  ADS  CAS  Google Scholar 

  21. Rose, K. D. & Emry, R. J. in Mammal Phylogeny: Placentals (eds Szalay, F. S., Novacek, M. J. & McKenna, M. C.) 81–102 (Springer, New York, 1993).

    Book  Google Scholar 

  22. Miyamoto, M. M. & Goodman, M. Biomolecular systematics of eutherian mammals: phylogenetic patterns and classification. Syst. Zool. 35, 230–240 (1986).

    Article  Google Scholar 

  23. Madsen, O. et al. Parallel adaptive radiations in two major clades of placental mammals. Nature (in the press).

  24. Eizirik, E., Murphy, W. J. & O'Brien, S. J. Molecular dating and biogeography of the early placental mammal radiation. J. Hered. (in the press).

  25. Hedges, S. B., Parker, P. H., Sibley, C. G. & Kumar, S. Continental breakup and the ordinal diversification of birds and mammals. Nature 381, 226–229 (1996).

    Article  ADS  CAS  Google Scholar 

  26. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25, 4876–4882 (1997).

    Article  CAS  Google Scholar 

  27. Swofford, D. L. PAUP* Phylogenetic Analysis using Parsimony and Other Methods (Sinauer, Sunderland, Massachusetts, 1998).

    Google Scholar 

  28. Strimmer, K. & Von Haeseler, A. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964–969 (1996).

    Article  CAS  Google Scholar 

  29. Kishino, H. & Hasegawa, M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29, 70–179 (1989).

    Article  Google Scholar 

  30. Templeton, A. R. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37, 221–244 (1983).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Hirschmann, M. Houck, R. Montali, R. Baker, G. Harris, K. Helgen, A. L. Roca, M. Roelke-Parker, A. Grafodatsky, O. Serov and T. Oleksyk for help in obtaining samples and technical assistance, and M. Smith and M. Dean for helpful suggestions. We also thank the NCI Frederick Molecular Technology Center for technical support, and the Advanced Biomedical Computer Center for computational assistance. All tissue samples were obtained with appropriate permits (CITES) issued to the National Cancer Institute, National Institutes of Health (principal officer, S.J.O). Y.P.Z. is supported by the Natural Science Foundation of China and Chinese Academy of Sciences. E.E. is supported by Conselho Nacional de Desenvolvimento Científico e Tecnológíco (CNPq), Brazil.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stephen J. O'Brien.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Murphy, W., Eizirik, E., Johnson, W. et al. Molecular phylogenetics and the origins of placental mammals. Nature 409, 614–618 (2001). https://doi.org/10.1038/35054550

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35054550

This article is cited by

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing