Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
Shopping Cart: ( empty )
You are here: Home > Journals > ZO > ZO08044
RESEARCH ARTICLE
Contents Vol 56(6)

A phylogeny and timescale for the living genera of kangaroos and kin (Macropodiformes : Marsupialia) based on nuclear DNA sequences

Robert W. Meredith A C , Michael Westerman B and Mark S. Springer A C
+ Author Affiliations
- Author Affiliations

A Department of Biology, University of California, Riverside, CA 92521, USA.

B Department of Genetics, La Trobe University, Bundoora, VIC 3083, Australia.

C Corresponding authors. Email: robert.meredith@email.ucr.edu; mark.springer@ucr.edu

Australian Journal of Zoology 56(6) 395-410 https://doi.org/10.1071/ZO08044
Submitted: 29 April 2008  Accepted: 5 February 2009   Published: 13 March 2009

Abstract

Kangaroos and kin (Macropodiformes) are the most conspicuous elements of the Australasian marsupial fauna. The approximately 70 living species can be divided into three families: (1) Hypsiprymnodontidae (the musky rat kangaroo); (2) Potoroidae (potoroos and bettongs); and (3) Macropodidae (larger kangaroos, wallabies, banded hare wallaby and pademelons). Here we examine macropodiform relationships using protein-coding portions of the ApoB, BRCA1, IRBP, Rag1 and vWF genes via maximum parsimony, maximum likelihood and Bayesian methods. We estimate times of divergence using two different relaxed molecular clock methods to present a timescale for macropodiform evolution and reconstruct ancestral states for grades of dental organisation. We find robust support for a basal split between Hypsiprymnodontidae and the other macropodiforms, potoroid monophyly and macropodid monophyly, with Lagostrophus as the sister-taxon to all other macropodids. Our divergence estimates suggest that kangaroos diverged from Phalangeroidea in the early Eocene, that crown-group Macropodiformes originated in the late Eocene or early Oligocene and that the potoroid–macropodid split occurred in the late Oligocene or early Miocene followed by rapid cladogenesis within these families 5 to 15 million years ago. These divergence estimates coincide with major geological and ecological changes in Australia. Ancestral state reconstructions for grades of dental organisation suggest that the grazer grade evolved independently on two different occasions within Macropodidae.


Acknowledgements

This work was partially supported by NSF (to MSS). We would like to thank Colleen Sims, Project officer of Project Eden, Shark Bay Office, WA and Nicole Noakes (same unit) for supplying tissue samples of Lagostrophus. We would also like to thank the Australian Museum (Sydney) for kindly making tissue samples of some species available to us. Lastly, we would like to thank two anonymous reviewers for their helpful comments and suggestions.


References

Amrine-Madsen, H. , Scally, M. , Westerman, M. , Stanhope, M. J. , Krajewski, C. , and Springer, M. S. (2003). Nuclear gene sequences provide evidence for the monophyly of australidelphian marsupials. Molecular Phylogenetics and Evolution 28, 186–196.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Aplin K. , and Archer M. (1987). Recent advances in marsupial systematics with a new syncretic classification. In ‘Possums and Opossums: Studies in Evolution’. (Ed. M. Archer.) pp. xv–lxxii. (Surrey Beatty & Sons: Chipping Norton.)

Archer M. (1984). The Australian marsupial radiation. In ‘Vertebrate Zoogeography and Evolution in Australasia’. (Eds M. Archer and G. Clayton.) pp. 633–808. (Hesperian Press: Perth.)

Archer, M. , Arena, R. , Bassarova, M. , Black, K. , and Brammall, J. , et al. (1999). The evolutionary history and diversity of Australian mammals. Australian Mammalogy 21, 1–45.
Baverstock P. R. , Krieg M. , and Birrell J. (1990). Evolutionary relationships of Australian marsupials as assessed by albumin immunology. In ‘Mammals from Pouches and Eggs: Genetics, Breeding and Evolution of Marsupials and Monotremes’. (Eds J. A. M. Graves, R. M. Hope and D. Cooper.) pp. 131–145. (CSIRO: Melbourne.)

Beck, R. , Godthelp, H. , Weisbecker, V. , Archer, M. , and Hand, S. J. (2008). Australia’s oldest marsupial fossils and their biogeographical implications. PLoS ONE 3, e1858.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Case J. A. (1989). Antarctica: the effect of high latitude heterochroneity on the origin of the Australian marsupials. In ‘Origins and Evolution of the Antarctic Biota’. (Ed. J. A. Crame.) pp. 217–226. Geological Society of America Special Publication 47.

Dawson T. J. (1989). Diets of macropodoid marsupials: general patterns and environmental influences. In ‘Kangaroos, Wallabies and Rat-kangaroos’. (Eds. G. Grigg, P. Jarman and I. Hume.) pp. 129–142. (Surrey Beatty & Sons: Chipping Norton.)

Dawson, L. , and Flannery, T. (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 larger wallabies. Australian Journal of Zoology 33, 473–498.
| Crossref | GoogleScholarGoogle Scholar | Eisenberg J. F. (1981). ‘The Mammalian Radiations.’ (University of Chicago Press: Chicago, IL.)

Farris, J. S. , Kallersjo, M. , Kluge, A. G. , and Bult, C. (1994). Testing significance of incongruence. Cladistics 10, 315–319.
| Crossref | GoogleScholarGoogle Scholar | Flannery T. F. (1984). Kangaroos: 15 million years of Australian bounders. In ‘Vertebrate Zoogeography and Evolution in Australasia’. (Eds M. Archer and G. Clayton.) pp. 817–836. (Hesperian Press: Carlisle.)

Flannery T. F. (1987). The relationships of the macropodoids (Marsupialia) and the polarity of some morphological features within Phalangeriformes. In ‘Possums and Opossums: Studies in Evolution’. (Ed. M. Archer) pp. 741–747. (Surrey Beatty & Sons: Chipping Norton.)

Flannery T. F. (1989). Phylogeny of the Macropodoidea: a study in convergence. In ‘Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 1–46. (Surrey Beatty & Sons: Chipping Norton.)

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. Journal of Paleontology 60, 418–447.
Freudenberger D. O. , Wallis I. R. , and Hume I. D. (1989). Phylogeny of the Macropodoidea: a study in convergence. In ‘Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 1–46. (Surrey Beatty & Sons: Chipping Norton.)

Godthelp, H. , Wroe, S. , and Archer, M. (1999). A new marsupial from the early Eocene Tingamarra Local Fauna of Murgon, southeastern Queensland: A prototypical Australian marsupial? Journal of Mammalian Evolution 6, 289–313.
| Crossref | GoogleScholarGoogle Scholar | Gradstein F. M. , Ogg J. G. , and Smith A. G. (2004). ‘A Geologic Timescale.’ (Cambridge University Press: Cambridge.)

Guindon, S. , and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Hume I. D. (1982). ‘Digestive Physiology and Nutrition of Marsupials.’ (Cambridge University 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. Australian Journal of Zoology 21, 28–46.
Marshall L. G. , Case J. A. , and Woodburne M. O. W. (1990). Phylogenetic relationships of the families of marsupials. In ‘Current Mammalogy Vol. 2’. (Ed. H. Genoways.) pp. 433–506. (Plenum Press: New York.)

Martin, H. A. (2006). Cenozoic climatic change and the development of the arid vegetation in Australia. Journal of Arid Environments 66, 533–563.
| Crossref | GoogleScholarGoogle Scholar | Rambaut A. (1996). Se-Al: Sequence Alignment Editor. Available at http://evolve.zoo.ox.ac.uk/ [Accessed August 2006].

Rambaut A. , and Drummond A. J. (2003). Tracer version 1.2 [computer program]. Available: http://evolve.zoo.ox.ac.uk [Accessed August 2006].

Rambaut, A. J. , and Drummond, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Sanson G. D. (1989). Morphological adaptations of teeth to diets and feeding in the Macropodoidea. In ‘Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 151–168. (Surrey Beatty & Sons: Chipping Norton, New South Wales.)

Schmelzle, T. , Sánchez-Villagra, M. R. , and Maier, W. (2007). Vestibular labyrinth diversity in diprotodontian marsupials. Mammal Study 32, 83–97.
| Crossref | GoogleScholarGoogle Scholar | Springer M. S. , Kirsch J. A. W. , and Case J. A. (1997). The chronicle of marsupial evolution. In ‘Molecular Evolution and Adaptive Radiation’. (Eds. T. J. Givnish, and K. J. Sytsma.) pp. 129–161. (Cambridge University Press: New York.)

Springer, M. S. , Burk-Herrick, A. , Meredith, R. , Eizirik, E. , Teeling, E. , O’Brien, S. J. , and Murphy, W. (2007). The adequacy of morphology for reconstructing the early history of placental mammals. Systematic Biology 56, 673–684.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Swofford D. L. (2002). ‘PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4.’ (Sinauer Associates, Sunderland, MA.)

Szalay F. S. (1994). ‘Evolutionary History of the Marsupials and an Analysis of Osteological Characters.’ (Cambridge University Press: New York.)

Tate, G. H. H. (1948). Results of the Archibald Expeditions. No. 59. Studies on the anatomy and phylogeny of the Macropodidae (Marsupialia). Bulletin of the American Museum of Natural History 91, 233–251.
Thomas O. (1888). ‘Catalogue of the Marsupialia and Monotremata in the Collection of the British Museum (Natural History)’. (British Museum of Natural History: London.)

Thorne, J. L. , and Kishino, H. (2002). Divergence time and evolutionary rate estimation with multilocus data. Systematic Biology 51, 689–702.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Tyndale-Biscoe H. (2005). ‘Life of Marsupials.’ (CSIRO Publishing: Melbourne.)

Van Gelder, R. G. (1977). Mammalian hybrids and generic limits. American Museum Novitates 2635, 1–25.
Wilson D. E. , and Reeder D. M. (2005). ‘Mammal Species of the World: a Taxonomic and Geographic Reference.’ (The Johns Hopkins University Press: Baltimore, MD.)

Woodburne M. O. (1984). Families of marsupials: relationships, evolution and biogeography. In ‘Mammals: Notes for a Short Course’. (Ed. T. W. Broadhead.) pp. 48–71. (University of Tennessee, Department of Geological Sciences Studies in Geology 8.)

Woodburne, M. O. , MacFadden, 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. Journal of Vertebrate Paleontology 13, 483–515.
Ziegler A. C. (1977). Evolution of New Guinea’s marsupial fauna in response to forested environment. In ‘The Biology of Marsupials’. (Eds B. Stonehouse and D. Gilmore.) pp. 117–138. (Macmillen: London.)