Abstract
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.
Similar content being viewed by others
LITERATURE CITED
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.
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.
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.
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.
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.
Baverstock, P. R., Richardson, B. J., Birrell, J., and Krieg, M. (1989). Albumin immunologic relationships of the Macropodidae (Marsupialia). Syst. Zool. 38: 38–50.
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.
Bishop, N. (1997). Functional anatomy of the macropodid pes. Proc. Linn. Soc. N.S.W. 117: 17–50.
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.
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.
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.
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.
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.
Cooke, B. N. (1997a). Two new balbarine kangaroos and lower molar evolution within the subfamily. Mem. Qld. Mus. 41: 269–280.
Cooke, B. N. (1997b). New Miocene bulungamayine kangaroos (Marsupialia: Potoroidae) from Riversleigh, northwestern Queensland. Mem. Qld. Mus. 41:281–294.
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.
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.
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.
Eisenberg, J. F. (1981). The Mammalian Radiations. University of Chicago Press, Chicago.
Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Hanahan, D. (1983). Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166: 557–580.
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.
Hayman, D. L. and Martin, P. G. (1974). Cytogenetics of marsupials. In: Comparative Mammalian Cytogenetics, K. Benirschke, ed., pp. 91–217, Springer, New York.
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.
Huelsenbeck, J. P., Bull, J. J., and Cunningham, C. W. (1996). Combining data in phylogenetic analysis. TREE 11: 152–158.
Hume, I. D. (1982). Digestive Physiology and Nutrition of Marsupials. Cambridge Univ. Press, New York.
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.
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.
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.
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.
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.
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.
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.
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.
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.
MacFadden, B. J. (1992). Fossil Horses: Systematics, Paleobiology, and Evolution of the Family Equidae. Cambridge University Press, New York, NY.
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.
Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982). Molecular Cloning. Cold Spring Harbory Laboratory Press, Cold Spring Harbor, New York.
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.
Megirian, D. (1992). Approaches to marsupial biochronology in Australia and New Guinea. Alcheringa 18: 259–274.
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.
Pearson, J. (1950a). A further note on the female urogenital system of Hypsiprymnodon moschatus (Marsupialia). Pap. Proc. R. Soc. Tasman. 1949: 203–209.
Pearson, J. (1950b). The relationships of the Potoroidae to the Macropodidae (Marsupialia). Pap. Proc. R. Soc. Tasman. 1949: 211–229.
Prideaux, G. J. (1999). Systematics & Evolution of the Extinct Kangaroo Subfamily, Sthenurinae. Ph.D. Dissertation. The Flinders University of South Australia.
Raven, H. C., and W. K. Gregory. (1946). Adaptive branching of the kangaroo family in relation to habitat. Am. Mus. Novit. 1309: 1–14.
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.
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.
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.
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.
Ride, W. D. L. (1993). Jackmahoneya gen. nov. and the genesis of the macropodiform molar. Mem. Assoc. Australas. Palaeontol. 15: 441–459.
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.
Rofe, R. H. (1978). G-banded chromosomes and the evolution of the Macropodidae. Aust. Mammal. 2: 53–64.
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.
Sanger, F., Nicklen, S., and Coulson, A. R. (1977). DNA sequencing with chain termination inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463–5467.
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.
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.
Sharman, G. B. (1961). The mitotic chromosomes of marsupials and their bearing on taxonomy and phylogeny. Aust. J. Zool. 9: 38–60.
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.
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.
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.
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.
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.
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.
Swofford, D. L. (1998). PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4, Sinauer Associates, Sunderland, Massachusetts.
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.
Szalay, F. S. (1994). The Evolutionary History of Marsupials and an Analysis of Osteological Characters. Cambridge Univ. Press, Cambridge, England.
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.
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.
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.
White, M. E. (1994). After the Greening: The Browning of Australia. New South Wales: Kangaroo Press.
Winge, H. (1941). The Inter-Relationships of the Mammalian Genera, Volume 1. Monotremata, Marsupialia, Insectivora, Chiroptera, Edentata. C. A. Reitzewls, ed., Forlag, Copenhagen, Denmark.
Woodburne, M. O. (1967). The Alcoota Fauna, Central Australia. An integrated palaeontological and geological study. Bull. Bur. Min. Res. Geol. Geophys. 87: 44–82.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Burk, A., Springer, M.S. Intergeneric Relationships Among Macropodoidea (Metatheria: Diprotodontia) and The Chronicle of Kangaroo Evolution. Journal of Mammalian Evolution 7, 213–237 (2000). https://doi.org/10.1023/A:1009488431055
Issue Date:
DOI: https://doi.org/10.1023/A:1009488431055