Parallel adaptive radiations in two major clades of placental mammals (original) (raw)

Nature volume 409, pages 610–614 (2001)Cite this article

Abstract

Higher level relationships among placental mammals, as well as the historical biogeography and morphological diversification of this group, remain unclear1,2,3. Here we analyse independent molecular data sets, having aligned lengths of DNA of 5,708 and 2,947 base pairs, respectively, for all orders of placental mammals. Phylogenetic analyses resolve placental orders into four groups: Xenarthra, Afrotheria, Laurasiatheria, and Euarchonta plus Glires. The first three groups are consistently monophyletic with different methods of analysis. Euarchonta plus Glires is monophyletic or paraphyletic depending on the phylogenetic method. A unique nine-base-pair deletion in exon 11 of the BRCA1 gene provides additional support for the monophyly of Afrotheria, which includes proboscideans, sirenians, hyracoids, tubulidentates, macroscelideans, chrysochlorids and tenrecids. Laurasiatheria contains cetartiodactyls, perissodactyls, carnivores, pangolins, bats and eulipotyphlan insectivores. Parallel adaptive radiations have occurred within Laurasiatheria and Afrotheria. In each group, there are aquatic, ungulate and insectivore-like forms.

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

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

Additional access options:

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. Shoshani, J. & McKenna, M. C. Higher taxonomic relationships among extant mammals based on morphology, with selected comparisons of results from molecular data. Mol. Phylogenet. Evol. 9, 572–584 (1998).
    Article CAS Google Scholar
  3. de Jong, W. W. Molecules remodel the mammalian tree. Trends Ecol. Evol. 13, 270–275 (1998).
    Article CAS Google Scholar
  4. Springer, M. S., Burk, A., Kavanagh, J. R., Waddell, V. G. & Stanhope, M. J. The interphotoreceptor retinoid binding protein gene in therian mammals: implications for higher level relationships and evidence for loss of function in the marsupial mole. Proc. Natl Acad. Sci. USA 94, 13754–13759 (1997).
    Article ADS CAS Google Scholar
  5. Springer, M. S. et al. Endemic African mammals shake the phylogenetic tree. Nature 388, 61–64 (1997).
    Article CAS Google Scholar
  6. 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
  7. Teeling, E. C. et al. Molecular evidence regarding the origin of echolocation and flight in bats. Nature 403, 188–192 (2000).
    Article ADS CAS Google Scholar
  8. Asher, R. J. A morphological basis for assessing the phylogeny of the ‘Tenrecoidea’ (Mammalia, Lipotyphla). Cladistics 15, 231–252 (1999).
    Google Scholar
  9. Luckett, W. P. & Hartenberger, J.-L. Monophyly or polyphyly of the order Rodentia: Possible conflict between morphological and molecular interpretations. J. Mammal. Evol. 1, 127–147 (1993).
    Article Google Scholar
  10. Waddell, P. J., Cao, Y., Hauf, J. & Hasegawa, M. Using novel phylogenetic methods to evaluate mammalian mtDNA, including amino acid-invariant sites-logdet plus site stripping, to detect internal conflicts in the data, with special reference to the positions of hedgehog, armadillo and elephant. Syst. Biol. 48, 31–53 (1999).
    Article CAS Google Scholar
  11. Penny, D., Masegawa, M., Waddell, P. J. & Hendy, M. D. Mammalian evolution: Timing and implications from using the logdeterminant transform for proteins of differing amino acid composition. Syst. Biol. 48, 76–93 (1999).
    Article CAS Google Scholar
  12. McKenna, M. C. & Bell, S. K. Classification of Mammals Above the Species Level (Columbia Univ. Press, New York, 1997).
    Google Scholar
  13. Rainger, R. Agenda for Antiquity: Henry Fairfield Osborn and Vertebrate Paleontology at the American Museum of Natural History, 1890–1935 (Univ. Alabama Press, Tuscaloosa, Alabama, 1991).
    Google Scholar
  14. Kumar, S. & Hedges, S. B. A molecular timescale for vertebrate evolution. Nature 392, 917–920 (1998).
    Article ADS CAS Google Scholar
  15. Foote, M., Hunter, J. P., Janis, C. M. & Sepkoski, J. J. Jr Evolutionary and preservational constraints on origins of biologic groups: divergence times of eutherian mammals. Science 283, 1310–1314 (1999).
    Article ADS CAS Google Scholar
  16. Rich, T. H. et al. A tribosphenic mammal from the Mesozoic of Australia. Science 278, 1438–1442 (1997).
    Article ADS CAS Google Scholar
  17. Mouchaty, 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 CAS Google Scholar
  18. 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
  19. Rasmussen, D. T. in The Evolution of Perissodactyls (eds Prothero, D. R. & Schoch, R. M.) 57–78 (Oxford Univ. Press, Oxford, 1989).
    Google Scholar
  20. Matthew, W. D. The Carnivora and Insectivora of the Bridger basin, middle Eocene. Mem. Am. Nat. Hist. 9, 291–567 (1909).
    Google Scholar
  21. Novacek, M. J. The skull of leptictid insectivorans and the higher-level classification of eutherian mammals. Bull. Am. Mus. Nat. Hist. 183, 1–111 (1986).
    Google Scholar
  22. Easteal, S. Molecular evidence for the early divergence of placental mammals. BioEssays 21, 1052–1058 (1999).
    Article CAS 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. Swofford, D. L., Olsen, G. P., Waddell, P. J. & Hillis, D. M. in Molecular Systematics (eds Hillis, D. M., Moritz, C. & Mable, B. K.) 407–492 (Sinauer, Sunderland, Massachusetts, 1996).
    Google Scholar
  25. Krajewski, C., Blacket, M., Buckley, L. & Westerman, M. A multigene assessment of phylogenetic relationships within the dasyurid marsupial subfamily Sminthopsinae. Mol. Phylogenet. Evol. 8, 236–248 (1997).
    Article CAS Google Scholar
  26. Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods) Version 4, (Sinauer, Sunderland, Massachusetts, 1998).
  27. Rambaut, A. & Grassly, N. C. Seq-Gen: An application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput. Appl. Biosci. 13, 303–306 (1997).
    CAS PubMed Google Scholar
  28. Rambaut, A. & Bromham, L. Estimating divergence dates from molecular sequences. Mol. Biol. Evol. 15, 442–448 (1998).
    Article CAS Google Scholar

Download references

Acknowledgements

We thank F. Catzeflis for tissue samples. This work was supported by the NSF (M.S.S.) and the TMR program of the European Commission (W.W.d.J.; M.J.S.).

Author information

Author notes

  1. Ole Madsen, Mark Scally and Wilfried W. de Jong: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Biochemistry, University of Nijmegen, PO Box 9101, Nijmegen, 6500 HB, The Netherlands
    Ole Madsen & Wilfried W. de Jong
  2. Department of Biology, University of California, Riverside, 92521, California, USA
    Mark Scally, Christophe J. Douady, Diana J. Kao, Heather M. Amrine & Mark S. Springer
  3. Queen's University of Belfast, Biology and Biochemistry, 97 Lisburn Road, Belfast, BT9 7BL, United Kingdom
    Mark Scally, Christophe J. Douady & Michael J. Stanhope
  4. Department of Biological Sciences, Box 210006, University of Cincinnati, Cincinnati, 45221, Ohio, USA
    Ronald W. DeBry
  5. Biology Department, University of Massachusetts, Amherst, 01003, Massachusetts, USA
    Ronald Adkins
  6. Graduate Group in Genetics, University of California, Riverside, 92521, California, USA
    Heather M. Amrine & Mark S. Springer
  7. Bioinformatics, SmithKline Beecham Pharmaceuticals, 1250 South Collegeville Road, UP1345, Collegeville, 19426, Pennsylvania, USA
    Michael J. Stanhope
  8. Institute for Biodiversity and Ecosystem Dynamics, Amsterdam, 1090 GT, The Netherlands
    Wilfried W. de Jong

Authors

  1. Ole Madsen
    You can also search for this author inPubMed Google Scholar
  2. Mark Scally
    You can also search for this author inPubMed Google Scholar
  3. Christophe J. Douady
    You can also search for this author inPubMed Google Scholar
  4. Diana J. Kao
    You can also search for this author inPubMed Google Scholar
  5. Ronald W. DeBry
    You can also search for this author inPubMed Google Scholar
  6. Ronald Adkins
    You can also search for this author inPubMed Google Scholar
  7. Heather M. Amrine
    You can also search for this author inPubMed Google Scholar
  8. Michael J. Stanhope
    You can also search for this author inPubMed Google Scholar
  9. Wilfried W. de Jong
    You can also search for this author inPubMed Google Scholar
  10. Mark S. Springer
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toMark S. Springer.

Supplementary information

Rights and permissions

About this article

Cite this article

Madsen, O., Scally, M., Douady, C. et al. Parallel adaptive radiations in two major clades of placental mammals.Nature 409, 610–614 (2001). https://doi.org/10.1038/35054544

Download citation

This article is cited by