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Evolution of the Monotremes: Phylogenetic Relationship to Marsupials and Eutherians, and Estimation of Divergence Dates Based on α-Lactalbumin Amino Acid Sequences

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Abstract

The amino acid sequences of the α-lactalbumins of the echidna, Tachyglossus aculeatus, and the platypus, Ornithorhynchus anatinus, were compared with each other and with those of 13 eutherian and 3 marsupial species. Phylogenetic parsimony analyses, in which selected mammalian lysozymes were used as outgroups, yielded trees whose consensus indicated that the two monotremes are sister taxa to marsupials and eutherians and that the latter two clades are each other's closest relatives. The data do not support the notion of a Marsupionta (monotreme–marsupial) clade. Pairwise comparison between the α-lactalbumins yielded maximum-likelihood distances from which divergence dates were estimated on the basis of three calibration points. The distance data support the view that the echidna and platypus lineages diverged from their last common ancestor at least 50 to 57 Ma (million years ago) and that monotremes diverged from marsupials and eutherian mammals about 163 to 186 Ma.

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LITERATURE CITED

  • Adachi, J. (1995). Ph.D. thesis, School of Mathematical and Physical Sciences, Tokyo.

  • Archer, M., Flannery, T., Ritchie, A. and Molnar, R. E. (1985). First Mesozoic mammal from Australia—An early Cretaceous monotreme. Nature 318: 363–366.

    Google Scholar 

  • Archer, M., Murray, P., Hand, S., and Godthelp, H. (1993). Reconsideration of monotreme relationships based on the skull and dentition of the Miocene Obdurodon dicksoni. In: Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 75–94, Springer-Verlag, New York.

    Google Scholar 

  • Benton, M. J. (1990). Phylogeny of the major tetrapod groups: Morphological data and divergence dates. J. Mol. Evol. 30: 409–424.

    Google Scholar 

  • Blackburn, D. G., Hayssen, V., and Murphy, C. J. (1989). The origins of lactation and the evolution of milk: A review with new hypotheses. Mammal. Rev. 19: 1–26.

    Google Scholar 

  • Catzeflis, F. M., Aguilar, J.-P., and Jaeger, J.-J. (1992). Muroid rodents: Phylogeny and evolution. Trends Ecol. Evol. 7: 122–126.

    Google Scholar 

  • Clemens, W. A., Richardson, B. J., and Baverstock, P. R. (1989). Biogeography and phylogeny of the Metatheria. In: Fauna of Australia, D. W. Walton and B. J. Richardson, eds., pp. 527–548, Australian Government Publishing Service, Canberra.

    Google Scholar 

  • Das Gupta, N. A., Alexander, L. K. J., and Beattie, C. W. (1992). The sequence of porcine cDNA encoding α-lactalbumin. Gene 110: 265–266.

    Google Scholar 

  • Easteal, S., and Herbert, G. (1997). Molecular evidence from the nuclear genome for the time frame of human evolution. J. Mol. Evol. 44(Suppl 1): S121–S132.

    Google Scholar 

  • Easteal, S., Collet, C., and Betty, D. (1995). The Mammalian Molecular Clock, Springer-Verlag, New York.

    Google Scholar 

  • Flannery, T. F., Archer, M., Rich, T. H., and Jones, R. (1995). A new family of monotremes from the Cretaceous of Australia. Nature 377: 418–420.

    Google Scholar 

  • Gemmell, N. J., and Westerman, M. (1994). Phylogenetic relationships within the class Mammalia: A study using mitochondrial 12S RNA sequences. J. Mammal. Evol. 2: 3–23.

    Google Scholar 

  • Gregory, W. K. (1947). The monotremes and the palimpsest theory. Bull. Am. Mus. Nat. Hist. 88: 1–52.

    Google Scholar 

  • Griffiths, M. (1978). The Biology of the Monotremes, Academic Press, New York.

    Google Scholar 

  • Griffiths, M., Wells, R. T., and Barrie, D. J. (1991). Observations on the skulls of fossil and extant echidnas (Monotremata: Tachyglossidae). Aust. Mammal. 14: 87–101.

    Google Scholar 

  • Grobler, J. A., Rao, K. R., Pervaiz, S., and Brew, K. (1994). Sequences of two highly divergent canine type c lysozymes: Implications for the evolutionary origins of the lysozyme/α-lactalbumin superfamily. Arch. Biochem. Biophys. 313: 360–366.

    Google Scholar 

  • Hill, R. T. L., and Brew, K. (1975). Lactose synthase. Adv. Enzymol. Rel. Areas Mol. Biol. 43: 411–489.

    Google Scholar 

  • Hope, R., Cooper, S., and Wainwright, B. (1990). Globin macromolecular sequences in marsupials and monotremes. Aust. J. Zool. 37: 289–313.

    Google Scholar 

  • Hu, Y., Wang, Y., Luo, Z., and Li, C. (1997). A new symmetrodont mammal from China and its implications for mammalian evolution. Nature 390: 137–142.

    Google Scholar 

  • Janke, A., Feldmaier-Fuchs, G., Thomas, W. K., von Haeseler, A., and Paabo, S. (1994). The marsupial mitochondrial genome and the evolution of placental mammals. Genetics 137: 243–256.

    Google Scholar 

  • Janke, A., Xu, X., and Arnason, U. (1997). The complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata, Marsupialia, and Eutheria. Proc. Natl. Acad. Sci. USA 94: 1276–1281.

    Google Scholar 

  • Jenkins, F. A., Jr. (1990). Monotremes and the biology of Mesozoic mammals. Neth. J. Zool. 40: 5–31.

    Google Scholar 

  • Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. CABIOS 8: 275–282.

    Google Scholar 

  • Kirsch, J. A. W., Lapointe, F.-J., and Springer, M. S. (1997). DNA-hybridisation studies of marsupials and their implications for metatherian classification. Aust. J. Zool. 45: 211–280.

    Google Scholar 

  • Kishino, H., and Hasegawa, M. (1989). Evolution of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data and the branching order in Hominidae. J. Mol. Evol. 29: 170–179.

    Google Scholar 

  • Kühne, W. G. (1973). The systematic position of monotremes reconsidered (Mammalia). Z. Morph. Tiere 75: 59–64.

    Google Scholar 

  • McKenzie, H. A., and White, F. H., Jr. (1991). Lysozyme and α-lactalbumin: Structure, function and interrelationships. Adv. Protein Chem. 41: 174–315.

    Google Scholar 

  • Messer, M., and Nicholas, K. R. (1991). Biosynthesis of marsupial milk oligosaccharides: Characterization and developmental changes of two galactosyltransferases in lactating mammary glands of the tammar wallaby, Macropus eugenii. Biochim. Biophys. Acta 1077: 79–85.

    Google Scholar 

  • Messer, M., Shaw, D. C., Weiss, A. S., Rismiller, P., and Griffiths, M. (1995). Amino acid sequence of echidna α-lactalbumin: Comparison with α-lactalbumin sequences of the platypus and other mammals; Estimation of divergence dates for monotremes. In: Proc. 7th FAOBMB Congr. (abstr.)

  • Messer, M., Griffiths, M., Rismiller, P. D., and Shaw, D. C. (1997). Lactose synthesis in a montreme, the echidna (Tachyglossus aculeatus): Isolation and amino acid sequence of echidna α-lactalbumin. Comp. Biochem. Physiol. B 118B: 403–410.

    Google Scholar 

  • Miyamoto, M. M., Kraus, F., Laipis, P. J., Tanhauser, S. M., and Webb, S. D. (1993). Mitochondrial DNA phylogenies within Artiodactyla. In: Mammal Phylogeny, F. S. Szalay, M. J., Novacek, and M. C. McKenna, eds., pp. 268–281, Springer-Verlag, New York.

    Google Scholar 

  • Murray, P. (1984). Furry egg-layers: The monotreme radiation. In: Vertebrate Zoogeography and Evolution in Australasia, M. Archer and G. Clayton, eds., pp. 571–583, Hesperian Press, Perth.

    Google Scholar 

  • Nitta, K., and Sugai, S. (1989). The evolution of lysozyme and α-lactalbumin. Eur. J. Biochem. 182: 111–118.

    Google Scholar 

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

    Google Scholar 

  • Novacek, M. J. (1993). Reflectlons on higher mammalian phylogenetics. J. Mammal. Evol. 1: 3–30.

    Google Scholar 

  • Pascual, R., Archer, M., Ortiz Jaureguizar, E., Prado, J. L., Godthelp, H., and Hand, S. J. (1992). The first non-Australian monotreme: An early Paleocene South American platypus. In: Platypus and Echidnas, M. Augee, ed., pp. 1–14, Royal Zoological Society of NSW, Sydney.

    Google Scholar 

  • Piotte, C. P., Marshall, C. J., Hubbard, M. J., Collett, C., and Grigor, M. R. (1997). Lysozyme and α-lactalbumin from the milk of a marsupial, the common brushtailed possum (Trichosurus vulpecula). Biochim. Biophys. Acta 1336: 235–242.

    Google Scholar 

  • Prager, E. M., and Jollès, P. (1996). Animal lysozymes c and g: An overview. In: Lysozymes: Model Enzymes in Biochemistry and Biology, P. Jollès, ed., pp. 9–31, Birkhauser Verlag, Basel.

    Google Scholar 

  • Qasba, P. K., and Kumar, S. (1997). Molecular divergence of lysozymes and α-lactalbumin. Crit. Rev. Biochem. Mol. Biol. 32: 255–306.

    Google Scholar 

  • Retief, J. D., Winkfein, R. J., and Dixon, G. H. (1993). Evolution of the monotremes. The sequences of the protamine P1 genes of platypus and echidna. Eur. J. Biochem. 218: 457–461.

    Google Scholar 

  • Richardson, B. J. (1988). A new view of the relationships of Australian and American marsupials. Aust. Mammal. 11: 71–73.

    Google Scholar 

  • Rowe, T. (1993). Phylogenetic systematics and the early history of mammals. In: Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 129–145, Springer-Verlag, New York.

    Google Scholar 

  • Sarich, V. M. (1985). Rodent macromolecular systematics. In: Evolutionary Relationships Among Rodents, W. P. Luckett and J.-L. Hartenberger, eds., pp. 423–452, Plenum Press, New York.

    Google Scholar 

  • Shaw, D. C., Messer, M., Scrivener, A. M., Nicholas, K. R., and Griffiths, M. (1993). Isolation, partial characterization and amino acid sequence of α-lactalbumin from platypus (Ornithorhynchus anatinus) milk. Biochim. Biophys. Acta 1161: 177–186.

    Google Scholar 

  • Springer, M. S., and Kirsch, J. A. W. (1993). A molecular phylogeny of placental mammals based on mitochondrial 12S rDNA sequences, with special reference to the problem of the Paenungulata. J. Mammal Evol. 1: 149–166.

    Google Scholar 

  • Springer, M. S., Westerman, M., and Kirsch, J. A. W. (1994). Relationships among orders and families of marsupials based on 12S ribosomal DNA sequences and the timing of the marsupial radiation. J. Mammal. Evol. 2: 85–115.

    Google Scholar 

  • Strimmer, K., and von Haeseler, A. (1996). Quartet puzzling: A quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13: 964–969.

    Google Scholar 

  • Swofford, D. L. (1993). PAUP: Phylogenetic Analysis Using Parsimony, Illinois Natural History Survey, Champaign.

    Google Scholar 

  • Westerman, M., and Edwards, D. (1991). The divergence between echidna (Monotremata: Tachyglossidae) and platypus (Monotremata: Ornithorhynchidae)—New data from DNA studies. Aust. Mammal. 14: 115–120.

    Google Scholar 

  • Westerman, M., Janczewski, D. N., and O'Brien, J. O. (1990). DNA-DNA hybridisation studies and marsupial phylogeny. Aust. J. Zool. 37: 315–323.

    Google Scholar 

  • Woodburne, M. O., Tedford, R. H., Archer, M., Turnbull, W. D., Plane, M. D., and Lundelius, E. L. (1985). Biochronology of the continental mammal record of Australia and New Guinea. Spec. Publ. S. Aust. Dept. Mines Energy 5: 347–363.

    Google Scholar 

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Authors
  1. Michael Messer
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  2. Anthony S. Weiss
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  3. Denis C. Shaw
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  4. Michael Westerman
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Messer, M., Weiss, A.S., Shaw, D.C. et al. Evolution of the Monotremes: Phylogenetic Relationship to Marsupials and Eutherians, and Estimation of Divergence Dates Based on α-Lactalbumin Amino Acid Sequences. Journal of Mammalian Evolution 5, 95–105 (1998). https://doi.org/10.1023/A:1020523120739

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