Journal of Mammalian Evolution

, Volume 7, Issue 4, pp 213–237 | Cite as

Intergeneric Relationships Among Macropodoidea (Metatheria: Diprotodontia) and The Chronicle of Kangaroo Evolution

  • Angela Burk
  • Mark S. Springer


The superfamily of kangaroos (Macropodoidea) is comprised of the subfamilies Propleopinae, Hypsiprymnodontinae, Paleopotoroinae, Potoroinae, Bulungamayinae, Balbarinae, Macropodinae, and Sthenurinae. Of these, Hypsiprymnodontinae, Potoroinae, and Macropodinae are extant. Competing phylogenetic hypotheses unite potoroines with either hypsiprymnodontines or macropodines, with most recent workers following a classificatory scheme that recognizes Hypsiprymnodontidae (hypsiprymnodontines) and Macropodidae (macropodines + potoroines). To address phylogenetic relationships among living macropodoids, we analyzed sequences from three mitochondrial genes (12S rRNA, tRNA valine, 16S rRNA) and one nuclear gene (protamine P1). MtDNA and protamine P1 both support a basal split of Hypsiprymnodon from other macropodoids rather than an association of Hypsiprymnodon with potoroines. This suggests that bipedal hopping and a complex stomach evolved once among macropodids. Monophyly of the Macropodinae is supported. Among macropodines, there is support for a Dorcopsis-Dorcopsulus association. Potoroine monophyly is less clear, although among potoroines there is support for an association of Bettongia and Aepyprymnus. Divergence times were estimated using 12S rRNA, tRNA-valine, and 16S rRNA transversions and suggest that kangaroos separated from a possum-like ancestor approximately 38–44 million years ago. Hypsiprymnodon diverged from other macropodoids approximately 34 to 38 million years ago. In agreement with the fossil record, the diversification of potoroines predates the diversification of macropodines. The latter have radiated in association with the development of a more arid climate and emergent grasslands over the Australian continent.

Kangaroo phylogeny Mitochondrial rRNA protamine P1 Macropodoidea Metatheria 


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  1. Anderson, S., de Bruijn, M. H. L., Coulson, A. R., Eperon, I. C., Sanger, F., and Young, I. G. (1982). Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J. Mol. Biol. 156: 683–717.Google Scholar
  2. Archer, M. (1984). The Australian mammal radiation. In: Vertebrate Zoogeography and Evolution in Australasia, M. Archer and G. Clayton, eds., pp. 633–808, Herperian Press, Carlisle, Western Australia.Google Scholar
  3. Archer, M. and Flannery, T. F. (1985). Revision of the extinct gigantic rat kangaroos (Potoroidae: Marsupialia) with a description of a new Miocene genus and species and a new Pleistocene species of Propleopus. J. Paleo. 9: 1331–1349.Google Scholar
  4. Archer, M., Godhelp, H., Hand, S. J., and Megirian, D. (1989). Fossil mammals of Riversleigh, Northwestern Queensland: Preliminary overview of biostratigraphy, correlation and environmental change. Aust. Zool. 25: 29–65.Google Scholar
  5. Arnason, U., Gullberg, A., Janke, A., and Xu, X. (1996). Pattern and timing of evolutionary divergences among hominoids based on analyses of complete mtDNA. J. Mol. Evol. 43: 650–661.Google Scholar
  6. Baverstock, P. R., Richardson, B. J., Birrell, J., and Krieg, M. (1989). Albumin immunologic relationships of the Macropodidae (Marsupialia). Syst. Zool. 38: 38–50.Google Scholar
  7. Bensley, B. A. (1903). On the evolution of the Australian Marsupialia; with remarks on the relationship of marsupials in general. Trans. Linn. Soc. Lond. 9: 83–217.Google Scholar
  8. Bishop, N. (1997). Functional anatomy of the macropodid pes. Proc. Linn. Soc. N.S.W. 117: 17–50.Google Scholar
  9. Burk, A. (1999). A Chronicle of Kangaroo Evolution: Phylogenetic Relationships Among Macropodoidea Based on Mitochondrial rRNA Genes with Implications for the Evolution of Morphological Characters. Ph.D. Dissertation, The University of California at Riverside.Google Scholar
  10. Burk, A., Westerman, M., and Springer, M. S. (1998). The phylogenetic position of the musky rat-kangaroo and the evolution of bipedal hopping in kangaroos (Macropodidae: Diprotodontia). Syst. Biol. 47: 457–474.Google Scholar
  11. Case, J. A. (1984). A new genus of Potoroinae (Marsupialia: Macropodidae) from the Miocene Ngapalakdi Local Fauna, South Australia, and a definition of the Potoroinae. J. Paleontol. 58: 1074–1086.Google Scholar
  12. Case, J. A. (1989). Antarctica: The effect of high latitude heterochroneity on the origin of the Australian marsupials. Geol. Soc. Spec. Publ. 47: 217–226.Google Scholar
  13. Case, J. A. (in press). Kyeema mahoneyi, Australia's oldest kangaroo from the Oligocene-Miocene Etadunna Formation, South Australia; and homologous trigon and trigonid morphologies in diprotodontian marsupials. J. Paleontology.Google Scholar
  14. Cooke, B. N. (1997a). Two new balbarine kangaroos and lower molar evolution within the subfamily. Mem. Qld. Mus. 41: 269–280.Google Scholar
  15. Cooke, B. N. (1997b). New Miocene bulungamayine kangaroos (Marsupialia: Potoroidae) from Riversleigh, northwestern Queensland. Mem. Qld. Mus. 41:281–294.Google Scholar
  16. Cooke, B. N. (1999). Wanburoo hilarus gen. et sp. nov., a lophodont bulungamayine kangaroo (Marsupialia: Macropodoidea: Bulungamayinae) from the Miocene deposits of Riversleigh, northwestern Queensland. Rec. West. Austr. Mus. Suppl. No. 57: 239–253.Google Scholar
  17. Dawson, L. and Flannery, T. F. (1985). Taxonomic and phylogenetic status of living and fossil kangaroos and wallabies of the genus Macropus Shaw (Macropodidae: Marsupialia) with a new subgeneric name for the large wallabies. Aust. J. Zool. 33: 473–498.Google Scholar
  18. Dawson, T. J. (1989). Diets of macropodoid marsupials: General patterns and environmental influences. In: Kangaroos, Wallabies and Rat-Kangaroos, G. Grigg, P. Jarman, and I. Hume, eds., pp. 129–142, Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  19. Eisenberg, J. F. (1981). The Mammalian Radiations. University of Chicago Press, Chicago.Google Scholar
  20. Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791.Google Scholar
  21. Flannery, T. F. (1984). Kangaroos: 15 million years of Australian bounders. In: Vertebrate Zoogeography and Evolution in Australasia, M. Archer and G. Clayton, eds., pp. 817–836, Herperian Press, Carlisle, Western Australia.Google Scholar
  22. Flannery, T. F. (1987). The relationships of the macropodoids (Marsupialia) and the polarity of some morphological features within the Phalangeriformes. In: Possums and Opossums: Studies in Evolution, M. Archer, ed., pp. 741–747, Surrey Beatty & Sons, New South Wales.Google Scholar
  23. Flannery, T. F. (1989). Phylogeny of the Macropodoidea: A study in convergence. In: Kangaroos, Wallabies and Rat-Kangaroos, G. Grigg, P. Jarman, and I. Hume, eds., pp. 1–46, Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  24. Flannery, T. F. and Archer, M. (1984). The macropodids (Marsupialia) of the early Pliocene Bow Local Fauna, central eastern New South Wales. Aust. Zool. 21:357–384.Google Scholar
  25. Flannery, T. F. and Archer, M. (1987). A new species of Hypsiprymnodon (Potoroidae: Marsupialia) from the Miocene of northwestern Queensland, and a reinterpretation of the morphology of the living Hypsiprymnodon moschatus. In: Possums and Opossums: Studies in Evolution, M. Archer, ed., pp. 749–767. Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  26. Flannery, T. F. and Hann, C. (1984). A new macropodine genus and species (Macropodidae: Marsupialia) from the early Pleistocene of southwestern Victoria. Aust. Mammal. 7: 193–205.Google Scholar
  27. Flannery, T. F. and Rich, T. H. R. (1986). Macropodoids of the middle Miocene Namba Formation, South Australia, and the homology of some dental structures in kangaroos. J. Paleontol. 60: 418–447.Google Scholar
  28. Flannery, T. F. and Szalay, F. S. (1982). Bohra paulae, a new giant fossil tree-kangaroo (Marsupialia: Macropodidae) from New South Wales, Australia. Aust. Mammal. 5: 38–54.Google Scholar
  29. Flannery, T. F., Archer, M., and Plane, M. (1983). Middle Miocene kangaroos (Macropodoidea: Marsupialia) from three localities in Northern Australia with a description of two new subfamilies. BMR J. Aust. Geol. Geophys. 7: 287–302.Google Scholar
  30. Flannery, T. F., Archer, M., and Plane, M. (1984). Phylogenetic relationships and a reconsideration of higher level systematics within the Potoroidae (Marsupialia). J. Paleontol. 58: 1087–1097.Google Scholar
  31. Flannery, T. F., Rich, T. H., Turnbull, W. D., and Lundelius, E. L. (1992). The Macropodoidea (Marsupialia) of the early Pliocene Hamilton Local Fauna, Victoria, Australia. Fieldiana: Geology 25: 1–37.Google Scholar
  32. Flannery, T. F., Boeadi, and Szalay, A. L. (1995). A new tree-kangaroo (Dendrolagus: Marsupialia) from Irian Jaya, Indonesia, with notes on ethnography and the evolution of tree-kangaroos. Mammalia 59: 65–84.Google Scholar
  33. Freudenberger, D. O., Wallis, I. R., and Hume, I. D. (1989). Digestive adaptations of kangaroos, wallabies and rat-kangaroos. In: Kangaroos, Wallabies and Rat-Kangaroos, G. Grigg, P. Jarman, and I. Hume, eds., pp. 179–187, Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  34. Hanahan, D. (1983). Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166: 557–580.Google Scholar
  35. Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating the human-ape split by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22: 160–174.Google Scholar
  36. Hayman, D. L. and Martin, P. G. (1974). Cytogenetics of marsupials. In: Comparative Mammalian Cytogenetics, K. Benirschke, ed., pp. 91–217, Springer, New York.Google Scholar
  37. Hillis, D. M., Mable, B. K., and Moritz, C. (1996). Applications of molecular systematics. In: Molecular Systematics, D. M. Hillis, C. Moritz, and B. K. Mable, eds., pp. 515–543, Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  38. Huelsenbeck, J. P., Bull, J. J., and Cunningham, C. W. (1996). Combining data in phylogenetic analysis. TREE 11: 152–158.Google Scholar
  39. Hume, I. D. (1982). Digestive Physiology and Nutrition of Marsupials. Cambridge Univ. Press, New York.Google Scholar
  40. Johnson, P. M., and Strahan, R. (1982). A further description of the musky rat-kangaroo, Hypsiprymnodon moschatus Ramsay, 1876 (Marsupialia: Potoroidae), with notes on its biology. Aust. Zool. 21: 28–46.Google Scholar
  41. Kirsch, J. A. W. (1977). A comparative serology of the Marsupialia, and a classification of the marsupials. Aust. J. Zool. Supp. Ser. No. 52: 1–152.Google Scholar
  42. Kirsch, J. A. W., Springer, M. S., Krajewski, C., Archer, M., Aplin, K., and Dickerman, A. W. (1990). DNA/DNA hybridization studies of carnivorous marsupials. I: The intergeneric relationships of bandicoots (Marsupialia: Perameloidea). J. Mol. Evol. 30: 434–448.Google Scholar
  43. Kirsch, J. A. W., Lapointe, F. J., and Foeste, A. (1995). Resolution of portions of the kangaroo phylogeny (Marsupialia: Macropodidae) using DNA hybridization. Biol. J. Linn. Soc. Lond. 55: 309–328.Google Scholar
  44. Kirsch, J. A. W., Lapointe, F. J., and Springer, M. S. (1997). DNA-hybridization studies of marsupials and their implications for metatherian classifications. Aust. J. Zool. 45: 211–280.Google Scholar
  45. Kishino, H., and Hasegawa, M. (1989). 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.Google Scholar
  46. Krajewski, C., Blacket, M., Buckley, L., and Westerman, M. (1997a). A multigene assessment of phylogenetic relationships within the dasyurid marsupial subfamily Sminthopsinae. Mol. Phylogenet. Evol. 8: 236–248.Google Scholar
  47. Krajewski, C., Young, J., Buckley, L., Woolley, P. A., and Westerman, M. (1997b). Reconstructing the evolutionary radiation of dasyurine marsupials with cytochrome b, 12S rRNA, and protamine gene trees. J. Mammal. Evol. 4: 217–236.Google Scholar
  48. Lockhart, P. J., Steel, M. A., Hendy, M. D., and Penny, D. (1994). Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. 11: 605–612.Google Scholar
  49. MacFadden, B. J. (1992). Fossil Horses: Systematics, Paleobiology, and Evolution of the Family Equidae. Cambridge University Press, New York, NY.Google Scholar
  50. MacPhail, M. K., Alley, N. F., Truswell, E. M., and Sluiter, I. R. K. (1994). Early Tertiary vegetation: evidence from spores and pollen. In: History of the Australian Vegetation: Cretaceous to Recent, R. S. Hill, ed., pp. 189–261, Cambridge University Press, Melbourne.Google Scholar
  51. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982). Molecular Cloning. Cold Spring Harbory Laboratory Press, Cold Spring Harbor, New York.Google Scholar
  52. Martin, H. A. (1994). Australian Tertiary phytogeography: Evidence from palynology. In: History of the Australian Vegetation: Cretaceous to Recent, R. S. Hill, ed., pp. 104–142, Cambridge University Press, Melbourne.Google Scholar
  53. Megirian, D. (1992). Approaches to marsupial biochronology in Australia and New Guinea. Alcheringa 18: 259–274.Google Scholar
  54. Pearson, J. (1946). The affinities of rat-kangaroos (Marsupialia) as revealed by a comparative study of the female urogenital system. Pap. Proc. R. Soc. Tasman. 1945: 13–25.Google Scholar
  55. Pearson, J. (1950a). A further note on the female urogenital system of Hypsiprymnodon moschatus (Marsupialia). Pap. Proc. R. Soc. Tasman. 1949: 203–209.Google Scholar
  56. Pearson, J. (1950b). The relationships of the Potoroidae to the Macropodidae (Marsupialia). Pap. Proc. R. Soc. Tasman. 1949: 211–229.Google Scholar
  57. Prideaux, G. J. (1999). Systematics & Evolution of the Extinct Kangaroo Subfamily, Sthenurinae. Ph.D. Dissertation. The Flinders University of South Australia.Google Scholar
  58. Raven, H. C., and W. K. Gregory. (1946). Adaptive branching of the kangaroo family in relation to habitat. Am. Mus. Novit. 1309: 1–14.Google Scholar
  59. Retief, J. D., Winkfein, R. J., Dixon, G. H., Adroer, R., Queralt, R., Ballabuga, R., and Oliva, R. (1993). Evolution of protamine P1 genes in primates. J. Molec. Evol. 37: 426–434.Google Scholar
  60. Retief, J. D., Krajewski, C., Westerman, M., and Dixon, G. H. (1995a). The evolution of protamine P1 genes in dasyurid marsupials. J. Mol. Evol. 41: 549–555.Google Scholar
  61. Retief, J. D., Krajewski, C., Westerman, M., Winkfein, R. J., and Dixon, G. H. (1995b). Molecular phylogeny and evolution of marsupial protamine P1 genes. Proc. R. Soc. Lond. B 259: 7–14.Google Scholar
  62. Richardson, B. J. and McDermid, E. M. (1978). A comparison of genetic relationships within the Macropodidae as determined from allozyme, cytological and immunological data. Aust. Mammal. 2: 43–52.Google Scholar
  63. Ride, W. D. L. (1993). Jackmahoneya gen. nov. and the genesis of the macropodiform molar. Mem. Assoc. Australas. Palaeontol. 15: 441–459.Google Scholar
  64. Ride, W. D. L., Pridmore, P. A., Barwick, R. E., Wells, R. T., and Heady, R. D. (1997). Towards a biology of Propleopus oscillans (Marsupialia: Propleopinae, Hypsiprymnodontidae). Proc. Linn. Soc. N.S.W. 117: 243–328.Google Scholar
  65. Rofe, R. H. (1978). G-banded chromosomes and the evolution of the Macropodidae. Aust. Mammal. 2: 53–64.Google Scholar
  66. Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B., and Erlich, H. A. (1988). Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491.Google Scholar
  67. Sanger, F., Nicklen, S., and Coulson, A. R. (1977). DNA sequencing with chain termination inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.Google Scholar
  68. Sanson, G. D. (1989). Morphological adaptations of teeth to diets and feeding in the Macropodoidea. In: Kangaroos, Wallabies and Rat-Kangaroos, G. Grigg, P. Jarman, and I. Hume, eds., pp. 151–168, Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  69. Seebeck, J. H., Bennett, A. F., and Scott, D. J. (1989). Ecology of the Potoroidae—A Review. In: Kangaroos, Wallabies and Rat-Kangaroos, G. Grigg, P. Jarman, and I. Hume, eds., pp. 67–88, Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  70. Sharman, G. B. (1961). The mitotic chromosomes of marsupials and their bearing on taxonomy and phylogeny. Aust. J. Zool. 9: 38–60.Google Scholar
  71. Smith, M. J., Hayman, D. L., and Hope, R. M. (1979). Observations on the chromosomes and reproductive systems of four macropodine interspecific hybrids (Marsupialia: Macropodidae). Aust. J. Zool. 27: 959–972.Google Scholar
  72. Springer, M. S., and Douzery, E. (1996). Secondary structure and patterns of evolution among mammalian mitochondrial 12S rRNA molecules. J. Mol. Evol. 43: 357–373.Google Scholar
  73. Springer, M. S. and Kirsch, J. A. W. (1991). DNA hybridization, the compression effect, and the radiation of diprotodontian marsupials. Syst. Zool. 40: 131–151.Google Scholar
  74. Springer, M. S. and Woodburne, M. O. (1989). The distribution of some basicranial characters within the Marsupialia and a phylogeny of the Phalangeriformes. J. Vertebr. Paleontol. 9: 210–221.Google Scholar
  75. Springer, M. S., Hollar, L. J., and Burk, A. (1995). Compensatory substitutions and the evolution of the mitochondrial 12S rRNA gene in mammals. Mol. Biol. Evol. 12: 1138–1150.Google Scholar
  76. Springer, M. S., Cleven, G. C., Madsen, O., de Jong, W. W., Waddell, V. G., Amrine, H. M., and Stanhope, M. J. (1997). Endemic African mammals shake the phylogenetic tree. Nature 388: 61–64.Google Scholar
  77. Swofford, D. L. (1998). PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4, Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  78. Swofford, D. L., Olsen, G. J., Waddell, P. J., and Hillis, D. M. (1996). Phylogenetic inference. In: Molecular Systematics, 2nd Edition, D. M. Hillis, C. Moritz, and B. K. Mable, eds., pp. 407–514, Sinauer, Sunderland, Massachusetts.Google Scholar
  79. Szalay, F. S. (1994). The Evolutionary History of Marsupials and an Analysis of Osteological Characters. Cambridge Univ. Press, Cambridge, England.Google Scholar
  80. Tate, G. H. H. (1948). Results of the Archbold Expeditions. No. 59. Studies on the anatomy and phylogeny of the Macropodidae (Marsupialia). Bull. Am. Mus. Nat. Hist. 91: 233–351.Google Scholar
  81. Thomas, O. (1904). On a collection of mammals made by Mr. J. T. Tunney in Arnhem Land, Northern Territory of South Australia. Novit. Zool. 11:222–229.Google Scholar
  82. Thompson, J. D., Higgins, G. D., and Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positive specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680.Google Scholar
  83. White, M. E. (1994). After the Greening: The Browning of Australia. New South Wales: Kangaroo Press.Google Scholar
  84. Winge, H. (1941). The Inter-Relationships of the Mammalian Genera, Volume 1. Monotremata, Marsupialia, Insectivora, Chiroptera, Edentata. C. A. Reitzewls, ed., Forlag, Copenhagen, Denmark.Google Scholar
  85. Woodburne, M. O. (1967). The Alcoota Fauna, Central Australia. An integrated palaeontological and geological study. Bull. Bur. Min. Res. Geol. Geophys. 87: 44–82.Google Scholar
  86. Woodburne, M. O. and Case, J. A. (1996). Dispersal, vicariance, and the Late Cretaceous to Early Tertiary land mammal biogeography from South America to Australia. J. Mammal. Evol. 3: 121–161.Google Scholar
  87. Woodburne, M. O., McFadden, B. J., Case, J. A., Springer, M. S., Pledge, N. S., Power, J. D., Woodburne, J. M., and Springer, K. B. (1993). Land mammal biostratigraphy and magnetostratigraphy of the Etadunna Formation (late Oligocene) of South Australia. J. Vertebr. Paleontol. 13: 483–515.Google Scholar
  88. Wroe, S., and Archer, M. (1995). Extraordinary diphyodonty-related change in dental function for a tooth of the extinct marsupial Ekaltadeta ima (Propleopinae, Hypsiprymnodontidae). Arch. Oral Biol. 40: 579–603.Google Scholar
  89. Wroe, S., Brammall, J., and Cooke, B. N. (1998). The skull of Ekaltadeta ima (Marsupialia, Hypsiprymnodontidae): an analysis of some marsupial cranial features and a re-investigation of propleopine phylogeny, with notes on the inference of carnivory in mammals. J. Paleontol. 72: 738–751.Google Scholar
  90. Ziegler, A. C. (1977). Evolution of New Guinea's marsupial fauna in response to a forested environment. In: The Biology of Marsupials, B. Stonehouse and D. P. Gilmore, eds., pp. 117–138, Macmillan, London.Google Scholar

Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • Angela Burk
    • 1
  • Mark S. Springer
    • 2
  1. 1.Department of BiologyUniversity of CaliforniaRiverside
  2. 2.Department of BiologyUniversity of CaliforniaRiverside

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