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Single origin of Malagasy Carnivora from an African ancestor

Abstract

The Carnivora are one of only four orders of terrestrial mammals living in Madagascar today. All four (carnivorans, primates, rodents and lipotyphlan insectivores) are placental mammals with limited means for dispersal, yet they occur on a large island that has been surrounded by a formidable oceanic barrier for at least 88 million years1,2, predating the age of origin for any of these groups3,4. Even so, as many as four colonizations of Madagascar have been proposed for the Carnivora alone5. The mystery of the island's mammalian origins is confounded by its poor Tertiary fossil record, which leaves us with no direct means for estimating dates of initial diversification. Here we use a multi-gene phylogenetic analysis to show that Malagasy carnivorans are monophyletic and thus the product of a single colonization of Madagascar by an African ancestor. Furthermore, a bayesian analysis6 of divergence ages for Malagasy carnivorans and lemuriforms indicates that their respective colonizations were temporally separated by tens of millions of years. We therefore conclude that a single event, such as vicariance or common dispersal, cannot explain the presence of both groups in Madagascar.

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Figure 1: Maximum likelihood phylogeny of Malagasy Carnivora and selected carnivoran outgroups.
Figure 2: Proposed biogeographical model of carnivoran dispersal from Africa.
Figure 3: Comparative age analysis of Lemuriformes and Malagasy Carnivora.
Figure 4: Comparison of bayesian age estimates for Malagasy carnivorans (above) and lemuriforms (below) relative to proposed landbridge temporal window8.

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References

  1. Coffin, M. F. & Rabinowitz, P. D. in Geology and Geophysics of Continental Margins (eds Watkins, J. S., Zhiqiang, F. & McMillen, K. J.) 207–246 (American Association of Petroleum Geologists, Tulsa, Oklahoma, 1992)

    Google Scholar 

  2. Storey, M. et al. Timing of hot-spot related volcanism and the breakup of Madagascar and India. Science 267, 852–855 (1995)

    Article  ADS  CAS  Google Scholar 

  3. Krause, D. W., Hartman, J. H. & Wells, N. A. in Natural Change and Human Impact in Madagascar (eds Goodman, S. M. & Patterson, B. D.) 3–43 (Smithsonian Institution Press, Washington DC, 1997)

    Google Scholar 

  4. Novacek, M. J. Mammalian phylogeny: Genes and supertrees. Curr. Biol. 11, R573–R575 (2001)

    Article  CAS  Google Scholar 

  5. Veron, G. La position systématique de Cryptoprocta ferox (Carnivora). Analyse cladistique des charactères morphologiques de carnivores Aeluroidea actuels et fossiles. Mammalia 59, 551–582 (1995)

    Article  Google Scholar 

  6. Thorne, J. L., Kishino, H. & Painter, I. S. Estimating the rate of evolution of the rate of evolution. Mol. Biol. Evol. 15, 1647–1657 (1998)

    Article  CAS  Google Scholar 

  7. Rowley, D. B. Age of initiation of collision between India and Asia: a review of stratigraphic data. Earth Planet. Sci. Lett. 145, 1–13 (1996)

    Article  ADS  CAS  Google Scholar 

  8. McCall, R. A. Implications of recent geological investigations of the Mozambique Channel for the mammalian colonization of Madagascar. Proc. R. Soc. Lond. B 264, 663–665 (1997)

    Article  ADS  CAS  Google Scholar 

  9. Rogers, R. R., Hartman, J. H. & Krause, D. W. Strategraphic analysis of Upper Cretaceous rocks in the Mahajanga Basin, northwestern Madagascar: implications for ancient and modern faunas. J. Geol. 108, 275–301 (2000)

    Article  ADS  CAS  Google Scholar 

  10. Arnason, U., Gullberg, A., Burguete, A. S. & Janke, A. Molecular estimates of primate divergences and new hypotheses for primate dispersal and the origin of modern humans. Hereditas 133, 217–228 (2000)

    Article  CAS  Google Scholar 

  11. Martin, R. D. Adaptive radiation and behaviour of Malagasy lemurs. Phil. Trans. R. Soc. Lond. B 264, 295–352 (1972)

    Article  ADS  CAS  Google Scholar 

  12. Simpson, G. G. Probabilities of dispersal in geologic time. Bull. Am. Mus. Nat. Hist. 99, 163–176 (1952)

    Google Scholar 

  13. Jansa, S. A., Goodman, S. M. & Tucker, P. K. Molecular phylogeny and biogeography of the native rodents of Madagascar (Muridae: Nesomyinae): a test of the single-origin hypothesis. Cladistics 15, 253–270 (1999)

    Article  Google Scholar 

  14. Olson, L. E. Systematics, Evolution, and Biogeography of Madagascar's Tenrecs (Mammalia: Tenrecidae). 349, PhD Thesis, Univ. Chicago (1999)

    Google Scholar 

  15. Yoder, A. D., Cartmill, M., Ruvolo, M., Smith, K. & Vilgalys, R. Ancient single origin of Malagasy primates. Proc. Natl Acad. Sci. USA 93, 5122–5126 (1996)

    Article  ADS  CAS  Google Scholar 

  16. Veron, G. & Catzeflis, F. M. Phylogenetic relationships of the endemic Malagasy carnivore Cryptoprocta ferox (Aeluroidea): DNA/DNA hybridization experiments. J. Mamm. Evol. 1, 169–185 (1993)

    Article  Google Scholar 

  17. Flynn, J. J. & Nedbal, M. A. Phylogeny of the Carnivora (Mammalia): congruence vs. incompatibility among multiple data sets. Mol. Phylogenet. Evol. 9, 414–426 (1998)

    Article  CAS  Google Scholar 

  18. Martin, R. D. Origins, diversity, and relationships of lemurs. Int. J. Primatol. 21, 1021–1049 (2000)

    Article  CAS  Google Scholar 

  19. Krause, D. W. et al. The Late Cretaceous vertebrate fauna of Madagascar: Implications for Gondwanan paleobiogeography. Geol. Soc. Am. Today 9, 1–7 (1999)

    Google Scholar 

  20. Krause, D. W. Fossil molar from a Madagascan marsupial. Nature 412, 497–498 (2001)

    Article  ADS  CAS  Google Scholar 

  21. Goodman, S. M., Ganzhorn, J. & Rakotondravony, D. in Natural History of Madagascar (eds Goodman, S. M. & Benstead, J.) (Univ. Chicago Press, Chicago, in the press)

  22. Albignac, R. Faune de Madagascar. 36 Mammifères carnivores, 206 (ORSTOM/CNRS, Paris, 1973)

    Google Scholar 

  23. Schmid, J. & Stephenson, P. J. in Natural History of Madagascar (eds Goodman, S. M. & Benstead, J.) (Univ. Chicago Press, Chicago, in the press)

  24. Kappeler, P. M. Lemur origins: rafting by groups of hibernators? Folia Primatol. (Basel) 71, 422–425 (2000)

    Article  CAS  Google Scholar 

  25. Yoder, A. D. in Biogéographie de Madagascar (ed. Lourenco, W. R.) 245–258 (Editions de l'ORSTOM, Paris, 1996)

    Google Scholar 

  26. Raxworthy, C. J., Forstner, M. R. & Nussbaum, R. A. Chameleon radiation by oceanic dispersal. Nature 415, 784–787 (2002)

    Article  ADS  CAS  Google Scholar 

  27. Swofford, D. L. PAUP*: phylogenetic analysis using parsimony (*and other methods) (Sinauer Associates, Sunderland, Massachusetts, 1998)

  28. Huelsenbeck, J. P. & Ronquist, F. MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)

    Article  CAS  Google Scholar 

  29. Maddison, W. P. & Maddison, D. R. MacClade: analysis of phylogeny and character evolution (Sinauer Associates, Sunderland, Massachusetts, 1992)

  30. Posada, D. & Crandall, K. A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818 (1998)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the authorities in Madagascar and the WWF for support of fieldwork, and L. Razafimanantsoa for access to tissues. We thank Z. Yang and M. Springer for discussion of methods, D. Krause for comments, and J. Thorne for guidance with his programs. This work was supported by the National Science Foundation, Washington, and the Field Museum's Pritzker Laboratory for Molecular Systematics. This is a Duke University Primate Center publication.

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Correspondence to Anne D. Yoder.

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Yoder, A., Burns, M., Zehr, S. et al. Single origin of Malagasy Carnivora from an African ancestor. Nature 421, 734–737 (2003). https://doi.org/10.1038/nature01303

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