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:

Endemic African mammals shake the phylogenetic tree

Abstract

The order Insectivora, including living taxa (lipotyphlans) and archaic fossil forms, is central to the question of higher-level relationships among placental mammals1. Beginning with Huxley2, it has been argued that insectivores retain many primitive features and are closer to the ancestral stock of mammals than are other living groups3. Nevertheless, cladistic analysis suggests that living insectivores, at least, are united by derived anatomical features4. Here we analyse DNA sequences from three mitochondrial genes and two nuclear genes to examine relationships of insectivores to other mammals. The representative insectivores are not monophyletic in any of our analyses. Rather, golden moles are included in a clade that contains hyraxes, manatees, elephants, elephant shrews and aardvarks. Members of this group are of presumed African origin5,6. This implies that there was an extensive African radiation from a single common ancestor that gave rise to ecologically divergent adaptive types. 12S ribosomal RNA transversions suggest that the base of this radiation occurred during Africa's window of isolation in the Cretaceous period before land connections were developed with Europe in the early Cenozoic era.

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

Access options

Buy this article

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

Figure 1: Majority-rule parsimony bootstrap trees based on mitochondrial (a), vWF (b), and A2AB (c) sequences.

Similar content being viewed by others

References

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

    Article  ADS  CAS  Google Scholar 

  2. Huxley, T. H. On the application of the laws of evolution to the arrangement of the Vertebrata, and more particularly to the Mammalia. Proc. R. Soc. Lond. 43, 649–662 (1880).

    Google Scholar 

  3. Matthew, W. D. The Carnivora and Insectivora of the Bridger Basin, Middle Eocene. Mem. Am. Mus. Nat. Hist. 9, 291–567 (1909).

    Google Scholar 

  4. MacPhee, R. D. E. & Novacek, M. J. in Mammal Phylogeny Vol. 2,Placentals(eds Szalay, F. S., Novacek, M. J. & McKenna, M. C.) 13–31 (Springer, New York, (1993)),

    Book  Google Scholar 

  5. Carroll, R. L. Vertebrate Paleontology and Evolution(Freeman, New York, (1988)).

    Google Scholar 

  6. Gheerbrant, E., Sudre, J. & Cappetta, H. APalaeocene proboscidean from Morocco. Nature 383, 68–70 (1996).

    Article  ADS  CAS  Google Scholar 

  7. Lavergne, A., Douzery, E., Stichler, T., Catzeflis, F. M. & Springer, M. S. Interordinal mammalian relationships: evidence for paenungulate monophyly is provided by complete mitochondrial 12S rRNA sequences. Mol. Phyl. Evol. 6, 245–258 (1996).

    Article  CAS  Google Scholar 

  8. Madsen, O., Deen, P. M. T., Pesole, G., Saccone, C. & de Jong, W. W. Molecular evolution of mammalian aquaporin-2: further evidence that elephant shrew and aardvark join the paenungulate clade. Mol. Biol. Evol. 14, 363–371 (1997).

    Article  CAS  Google Scholar 

  9. Porter, C. A., Goodman, M. & Stanhope, M. J. Evidence on mammalian phylogeny from sequences of exon 28 of the von Willebrand factor gene. Mol. Phys. Evol. 5, 89–101 (1996).

    Article  CAS  Google Scholar 

  10. Stanhope, M. J. et al. Mammalian evolution and the interphotoreceptor retinoid binding protein (IRBP) gene: convincing evidence for several superordinal clades. J. Mol. Evol. 43, 83–92 (1996).

    Article  ADS  CAS  Google Scholar 

  11. Cope, E. D. The condylarthra. Am. Nat. 18, 790–805, 892–906 (1884).

    Article  Google Scholar 

  12. Fischer, M. S. & Tassy, P. in Mammal Phylogeny Vol. 2,Placentals(eds Szalay, F. S., Novacek, M. J. & McKenna, M. C.) 217–234 (Springer, New York, (1993)).

    Book  Google Scholar 

  13. de Jong, W. W., Zweers, A. & Goodman, M. Relationship of aardvark to elephants, hyraxes and sea cows from α-crystallin sequences. Nature 292, 538–540 (1981).

    Article  ADS  CAS  Google Scholar 

  14. de Jong, W. W., Leunissen, J. A. M. & Wistow, G. J. in Mammal Phylogeny Vol. 2,Placentals(eds Szalay, F. S., Novacek, M. J. & McKenna, M. C.) 5–12 (Springer, New York, (1993)).

    Book  Google Scholar 

  15. Faith, D. P. Cladistic permutation tests for monophyly and nonmonophyly. Syst. Zool. 40, 366–375 (1991).

    Article  Google Scholar 

  16. 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, 170–179 (1989).

    Article  ADS  CAS  Google Scholar 

  17. Glover, T. D. Aspects of sperm production in some east African mammals. J. Reprod. Fertil. 35, 45–53 (1973).

    Article  CAS  Google Scholar 

  18. Hartenberger, J. L. Hypothese paleontologique sur l'origine des Macroscelidea (Mammalia). C.R. Acad. Sci. 302, 247–249 (1986).

    Google Scholar 

  19. Novacek, M. in Macromolecular Sequences in Systematic and Evolutionary Biology(ed. Goodman, M.) 3–41 (Plenum, New York, (1982)).

    Book  Google Scholar 

  20. Sibley, C. G. & Ahlquist, J. E. Reconstructing bird phylogeny by comparing DNAs. Sci. Am. 254, 82–92 (1986).

    Article  CAS  Google Scholar 

  21. 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 

  22. Springer, M. S., Hollar, L. J. & Burk, A. Compensatory substitutions and the evolution of the mitochondrial 12S rRNA gene in mammals. Mol. Biol. Evol. 12, 1138–1150 (1995).

    CAS  PubMed  Google Scholar 

  23. Thompson, J. D., Higgins, G. D. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    Article  CAS  Google Scholar 

  24. Springer, M. S. & Douzery, D. Secondary structure and patterns of evolution among mammalian mitochondrial 12S rRNA molecules. J. Mol. Evol. 43, 357–373 (1996).

    Article  ADS  CAS  Google Scholar 

  25. De Rijk, P., Van de Peer, Y., Chapelle, S. & De Wachter, R. Nucleic Acids Res. 22, 3495–3501 (1994).

    Google Scholar 

  26. Swofford, D. L., Olsen, G. J., Waddell, P. J. & Hillis, D. M. in Molecular Systematics(eds Hillis, D. M., Moritz, C. & Mable, B. K.) 407–514 (Sinauer, Sunderland, MA, (1996)).

    Google Scholar 

  27. Tamura, K. & Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526 (1993).

    CAS  PubMed  Google Scholar 

  28. Lockhart, P. J., Steel, M. A., Hendy, M. D. & Penny, D. Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. 11, 605–612 (1994).

    CAS  PubMed  Google Scholar 

  29. Hasegawa, M., Kishino, H. & Yano, T. Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 21, 160–174 (1985).

    Article  ADS  Google Scholar 

  30. Arnason, U., Gullberg, A., Janke, A. & Xu, X. Pattern and timing of evolutionary divergences among hominoids based on analyses of complete mtDNAs. J. Mol. Evol. 43, 650–661 (1996).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Alfred P. Sloan Foundation, the European Commission, the NSF, the Nuffield Foundation and the Royal Society. We thank D. Willemsen for technical assistance, D. Swofford for permission to use PAUP 4.0d52-54, and F. Catzeflis, E. Harley, J. Kirsch, G. Olbricht, J. Wensing and the Noorder Zoo for tissue samples.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark S. Springer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Springer, M., Cleven, G., Madsen, O. et al. Endemic African mammals shake the phylogenetic tree. Nature 388, 61–64 (1997). https://doi.org/10.1038/40386

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/40386

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