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Phylogenetic analysis of the perissodactylan family Tapiridae using mitochondrial cytochromec oxidase (COII) sequences

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Abstract

The four extant members of the family Tapiridae have a disjunct, relictual distribution, with three species being Neotropical (Tapirus bairdii, T. terrestris, andT. pinchaque) and one found in Southeast Asia (T. indicus). Little recent work on tapir systematics have appeared, and no molecular studies of this group have been published. A phylogenetic analysis was undertaken using sequences of the mitochondrial cytochromec oxidase subunit II gene (COII) from representatives of the four species of tapirs, as well as a representative outgroup,Equus caballus. Analyses of the COII sequences indicate a close relationship between the two South American species of tapirs,T. terrestris andT. pinchaque, and estimates of divergence dates using rates of COII evolution are compatible with migration of a single tapir lineage into South America following the emergence of the isthmus of Panama, about 3 million years bp. Various methods of analysis, including maximum parsimony, maximum likelihood, and neighbor-joining, provided poorer resolution of other tapir relationship. The COII data suggest that three distinct tapir mitochondrial lineages, a South American (represented byT. terrestris andT. pinchaque), a Central American (represented byT. bairdii), and an Asian (represented byT. indicus) diverged relatively rapidly, 20–30 million years bp. Another goal of this study was to calibrate the rate of COII evolution in a eutherian mammal group which has a good fossil record, such as perissodactyls, to estimate accurately the rate of COII evolution in a nonprimate mammalian group. The rate of COII evolution in equids and tapirs has been relatively constant and, using corrected distances, calibrated to be approximately 0.22% lineage/million years. This rate is three-to fourfold lower than that of hominoid primates.

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Literature Cited

  • Adkins, R. M., and Honeycutt, R. L. (1994). Evolution of the primate cytochromec oxidase subunit II gene.J. Mol. Evol. 38: 215–231.

    PubMed  Google Scholar 

  • Amato, G. D., Ashley, M. V., and Gatesy, J. (1993). Molecular evolution inliving species of rhinoceros: Implications for conservation. In:Proceedings of an International Conference: Rhinoceros Biology and Conservation, O. A. Ryder, eds., pp. 114–122, Zoological Society of San Diego.

  • Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H. L., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., Schreier, P. H., Smith, A. J. H., Staden, R., and Young, I. G. (1981). Sequence and organization of the human mitochondrial genome.Nature 290: 457–465.

    PubMed  Google Scholar 

  • Anderson, W., De Bruijn, M. H. L., Coulson, A. R., Eperon, I. C., Sanger, F., and Young, I. G. (1982). Complete sequence of bovine mitochrondrial DNA: Conserved features of the mammalian mitochondrial genome.J. Mol. Biol. 156: 683–717.

    PubMed  Google Scholar 

  • Ashley, M. V., and Vaughn, J. L. (1995). Owl monkeys (Aotus) are highly divergent in mitochondrial cytochromec oxidase (COII) sequences.Int. J. Primatal. 16: 793–806.

    Google Scholar 

  • Ashley, M. V., Melnick, D. J., and Western, D. (1990). Conservation genetics of the black rhinoceros (Diceros bicornis). I. Evidence from the mitochondrial DNA of three populations.Conserv. Biol. 4: 71–77.

    Google Scholar 

  • Baba, M. L., Darga, L. L., Goodman, M., and Czelusniak, J. (1981). Evolution of cytochromec investigated by the maximum parsimony method.J. Mol. Evol. 17: 197–213.

    PubMed  Google Scholar 

  • Bremer, K. (1994). Branch support and tree stability.Cladistics 10: 295–304.

    Google Scholar 

  • Brown, G. G., and Simpson, M. V. (1982). Novel features of animal mtDNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes.Proc. Natl. Acad. Sci. USA 79: 3246–3250.

    PubMed  Google Scholar 

  • Cann, R. L., Brown, W. M., and Wilson, A. C. (1984). Polymorphic sites and the mechanism of evolution in human mitochondrial DNA.Genetics 106: 479–499.

    PubMed  Google Scholar 

  • Capraldi, R. A. (1990). Structure and function of cytochromec oxidase.Annu. Rev. Biochem. 59: 569–596.

    PubMed  Google Scholar 

  • Disotell, T. R., Honeycutt, R. L., and Ruvolo, M. (1992). Mitochondrial DNA phylogeny of the Old-World monkey tribe Papionini.Mol. Biol. Evol. 9: 1–13.

    PubMed  Google Scholar 

  • Donaghue, M. J., Olmstead, R. G., Smith, J. F., and Palmer, J. D. (1992). Phylogenetic relationships of Dipsacales based onrbcL sequences.Ann. Mo. Bot. Gard. 79: 333–345.

    Google Scholar 

  • Douzery, E., and Catzeflis, F. M. (1995). Molecular evolution of the mitochondrial 12S rRNA in Ungulata (Mammalia).J. Mol. Evol. 41: 622–636.

    PubMed  Google Scholar 

  • Eisenberg, J. F., Groves, C. P., and MacKinnon, K. (1987). Tapire. In:Grzimeks Enzyklopadie, W. Keienburg, ed., Vol. 4, pp. 598–608, Kindler Verlag, Munich.

    Google Scholar 

  • Felsenstein, J. (1981). Evolutionary trees from DNA sequences: A maximum likelihood approach.J. Mol. Evol. 17: 368–376.

    PubMed  Google Scholar 

  • Felsenstein, J. (1993).PHYLIP (Phylogeny Inference Package). Version 3.5c, University of Washington, Seattle.

    Google Scholar 

  • Flint, J., Taylor, A. M., and Clegg, J. B. (1988). Structure and evolution of the horse ξ globin lucus.J. Mol. Biol. 199: 427–437.

    PubMed  Google Scholar 

  • Flint, J., Ryder, O. A., and Clegg, J. B. (1990). Comparison of the α-globin gene cluster structure in Perissodactyla.J. Mol. Evol. 30: 36–42.

    Google Scholar 

  • George, M., and Ryder, O. A. (1986). Mitochondrial DNA evolution in the genusEquus.Mol. Biol. Evol. 3: 535–546.

    PubMed  Google Scholar 

  • Hershkovitz, P. (1954). Mammals of Northern Colombia, Prelimimary Report No. 7: Tapirs (genusTapirus), with a systematic review of American species.Proc. U. S. Natl. Mus. Smith. Inst. 103: 465–496.

    Google Scholar 

  • Honeycutt, R. L., Nedbal, M. A., Adkins, R. M., and Janecek, L. L. (1995). Mammalian mitochondrial DNA evolution: A comparison of the cytochromeb and cytochromec oxidase II genes.J. Mol. Evol. 40: 260–272.

    PubMed  Google Scholar 

  • Irwin, D. M., Kocher, T. D., and Wilson, A. C. (1991). Evolution of the cytochromeb gene of mammals.J. Mol. Evol. 32: 128–144.

    PubMed  Google Scholar 

  • Ishida, N., Oyunsuren, T., Mashima, S., Mukoyama, H., and Saitou, N. (1995). Mitochondrial DNA sequences of various species of the genusEquus with special reference to the phylogenetic relationship between Przewalskii's wild horse and domestic horse.J. Mol. Evol. 41: 180–188.

    PubMed  Google Scholar 

  • Jama, M., Zhang, Y., Aman, R. A., and Ryder, O. A. (1993). Sequence of the mitochondrial control region, trRNATHR, tRNAPRO and tRNAPHE genes from the black rhinoceros,Diceros bicornis.Nucleic Acids Res. 21: 4392.

    PubMed  Google Scholar 

  • Kurten, B., and Anderson, E. (1980).Pleistocene Mammals of North America, Columbia University Press, New York.

    Google Scholar 

  • Luntz, T. L., and Margoliash, E. (1988). An amino acid sequence region of subunit II of cytochrome oxidase which may be responsible for evolutionary changes in reactivity with different cytochromesc. In:Cytochrome Systems: Molecular Biology and Bioenergetics, S. Papa, B. Changes, and L. Ernster, eds., pp. 271–279, Plenum, New York.

    Google Scholar 

  • MacFadden, B. J. (1992).Fossil Horses: Systematics, Paleobiology, and Evolution of the Family Equidae, Cambridge University Press, Cambridge.

    Google Scholar 

  • Maddison, W. P., and Maddison, D. R. (1992).MacClade. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Merenlender, A. M., Woodruff, D. S., Ryder, O. A., Kock, R., and Vahala, J. (1989). Allozyme variation and differentiation in African and Indian rhonoceroses.J. Hered. 80: 377–381.

    PubMed  Google Scholar 

  • Morales, J. C., and Melnick, D. J. (1994). Molecular systematics of the living rhinoceros.Mol. Phylo. Evol. 3: 128–134.

    Google Scholar 

  • Nowak, R. M. (1991).Walker's Mammals of the World, Vol. II, 5th ed., John Hopkins University Press, Baltimore.

    Google Scholar 

  • O'Ryan, C., and Harley, E. H. (1993). Comparisons of mitochondrial DNA in black and white rhinoceroses.J. Mammal. 74: 343–346.

    Google Scholar 

  • Osheroff, N., Speck, S. H., Margoliash, E., Veerman, E. C. I., Wilms, J., Konig, B. W., and Muijsers, A. O. (1983). The reaction of primate cytochromesc with cytochromec oxidase.J. Biol. Chem. 258: 5731–5738.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Prothere, D. R., and Schoch, R. M. (eds.) (1989).The Evolution of Perissodactyls, Clarendon Press, New York.

    Google Scholar 

  • Ramharack, R., and Deeley, R. G. (1987). Structure and evolution of primate cytochromec oxidase subunit II gene.J. Biol. Chem. 262: 14014–14021.

    PubMed  Google Scholar 

  • Ray, C. E., and Sanders, A. E. (1984). Pleistocene tapirs in the Eastern United States. In:Contributions in Quaternary Vertebrate Paleontology: A Volume in Memorial to John E. Guilday, H. H. Genoways and M. R. Dawson, eds., Vol. 8, pp. 283–315, Spec. Publ. Carnegie Mus. Nat. Hist.

  • Ruvolo, M., Zehr, S., von Dornum, M., Pan, D., Chang, B., and Lin, J. (1993). Mitochondrial COII sequences and modern human origins.Mol. Biol. Evol. 10: 1115–1135.

    PubMed  Google Scholar 

  • Ruvolo, M., Disotell, T. R., Allard, M. W., Brown, W. M., and Honeycutt, R. L. (1991). Resolution of the African hominoid tricotomy by use of a mitochondrial gene sequence.Proc. Natl. Acad. Sci. USA 88: 1570–1574.

    PubMed  Google Scholar 

  • Ryder, O. A., and Chemnick, L. G. (1990). Chromosomal and molecular evolution in Asiatic wild asses.Genetica 83: 67–72.

    PubMed  Google Scholar 

  • Saitou, N., and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees.Mol. Biol. Evol. 4: 406–425.

    PubMed  Google Scholar 

  • Sarich, V. M., and Wilson, A. C. (1967). Immunological time scale for hominid evolution.Science 158: 1200–1203.

    PubMed  Google Scholar 

  • Schoch, R. M. (1989). A review of the tapiroids. In:The Evolution of Perissodactyls, D. R. Prothero and R. M. Schoch, Eds., pp. 299–320, Oxford University Press, New York.

    Google Scholar 

  • Swofford, D. L. (1991).PAUP: Phylogenetic Analysis Using Parsimony, Illinois Natural History Survey, Champaign.

    Google Scholar 

  • Taha, T. S. M., and Ferguson-Miller, S. (1992). Interaction of cytochromec with cytochromec oxidase studied by monoclonal antibodies and a protein modifying reagent.Biochemistry 31: 9090–9097.

    PubMed  Google Scholar 

  • Tajima, F. (1993). Simple methods for testing the molecular evolutionary clock hypothesis.Genetics 135: 599–607.

    PubMed  Google Scholar 

  • Wichman, H. A., Payne, C. T., Ryder, O. A., Hamilton, M. J., Maltbie, M., and Baker, R. J. (1991). Genomic distribution of heterochromatic sequences in equids: Implications to rapid chromosomal evolution.J. Hered. 82: 369–377.

    PubMed  Google Scholar 

  • Xu, X., and Árnason, Ú. (1994). The complete mitochondrial DNA sequence of the horse,Equus caballus: Extensive heteroplasmy of the control region.Gene 148: 357–362.

    PubMed  Google Scholar 

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Ashley, M.V., Norman, J.E. & Stross, L. Phylogenetic analysis of the perissodactylan family Tapiridae using mitochondrial cytochromec oxidase (COII) sequences. J Mammal Evol 3, 315–326 (1996). https://doi.org/10.1007/BF02077448

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