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Molecular phylogenetics and the origins of placental mammals

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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.

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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.

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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 

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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.

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Author notes

  1. William J. Murphy, Eduardo Eizirik and Oliver A. Ryder: These authors contributed equally to this work

Authors and Affiliations

  1. Laboratory of Genomic Diversity, National Cancer Institute, Frederick, 21702, Maryland, USA

    William J. Murphy, Eduardo Eizirik, Warren E. Johnson & Stephen J. O'Brien

  2. Key Laboratory of Cellular and Molecular Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

    Ya Ping Zhang

  3. Center for Reproduction of Endangered Species, Zoological Society of San Diego, San Diego, 92112, California, USA

    Oliver A. Ryder

  4. Department of Biology, University of Maryland, College Park, 20742, Maryland, USA

    Eduardo Eizirik

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  1. William J. Murphy
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  2. Eduardo Eizirik
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  4. Ya Ping Zhang
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  5. Oliver A. Ryder
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  6. Stephen J. O'Brien
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Correspondence to Stephen J. O'Brien.

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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

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