Journal of Mammalian Evolution

, Volume 15, Issue 1, pp 1–36 | Cite as

A Phylogeny and Timescale for Marsupial Evolution Based on Sequences for Five Nuclear Genes

Original Paper

Abstract

Even though marsupials are taxonomically less diverse than placentals, they exhibit comparable morphological and ecological diversity. However, much of their fossil record is thought to be missing, particularly for the Australasian groups. The more than 330 living species of marsupials are grouped into three American (Didelphimorphia, Microbiotheria, and Paucituberculata) and four Australasian (Dasyuromorphia, Diprotodontia, Notoryctemorphia, and Peramelemorphia) orders. Interordinal relationships have been investigated using a wide range of methods that have often yielded contradictory results. Much of the controversy has focused on the placement of Dromiciops gliroides (Microbiotheria). Studies either support a sister-taxon relationship to a monophyletic Australasian clade or a nested position within the Australasian radiation. Familial relationships within the Diprotodontia have also proved difficult to resolve. Here, we examine higher-level marsupial relationships using a nuclear multigene molecular data set representing all living orders. Protein-coding portions of ApoB, BRCA1, IRBP, Rag1, and vWF were analyzed using maximum parsimony, maximum likelihood, and Bayesian methods. Two different Bayesian relaxed molecular clock methods were employed to construct a timescale for marsupial evolution and estimate the unrepresented basal branch length (UBBL). Maximum likelihood and Bayesian results suggest that the root of the marsupial tree is between Didelphimorphia and all other marsupials. All methods provide strong support for the monophyly of Australidelphia. Within Australidelphia, Dromiciops is the sister-taxon to a monophyletic Australasian clade. Within the Australasian clade, Diprotodontia is the sister taxon to a Notoryctemorphia + Dasyuromorphia + Peramelemorphia clade. Within the Diprotodontia, Vombatiformes (wombat + koala) is the sister taxon to a paraphyletic possum group (Phalangeriformes) with kangaroos nested inside. Molecular dating analyses suggest Late Cretaceous/Paleocene dates for all interordinal divergences. All intraordinal divergences were placed in the mid to late Cenozoic except for the deepest splits within the Diprotodontia. Our UBBL estimates of the marsupial fossil record indicate that the South American record is approximately as complete as the Australasian record.

Keywords

Marsupialia Phylogeny Fossil record Molecular divergence dates Ameridelphia Australidelphia Unrepresented basal branch length 

Supplementary material

References

  1. Abbie AA (1937) Some observations on the major subdivisions of the Marsupialia, with special reference to the position of the Peramelidae and Caenolestidae. J Anat 71:424–436Google Scholar
  2. Adam P (1999) Australian rainforests. Oxford University Press, OxfordGoogle Scholar
  3. Amrine-Madsen H, Scally M, Westerman M, Stanhope MJ, Krajewski C, Springer MS (2003) Nuclear gene sequences provide evidence for the monophyly of australidelphian marsupials. Mol Phylogenet Evol 28:186–196PubMedCrossRefGoogle Scholar
  4. Aplin KP, Archer M (1987) Recent advances in marsupial systematics with a new syncretic classification. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons, Chipping Norton, New South Wales, pp xv–xxiiGoogle Scholar
  5. Archer M (1982) Review of the dasyurid (Marsupialia) fossil record, integration of data bearing on phylogenetic interpretation, and suprageneric classification. In: Archer M (ed) Carnivorous marsupials. Royal Zoological Society of New South Wales, Mossman, New South Wales, pp. 397–443Google Scholar
  6. Archer M, Hand SJ (2006) The Australian marsupial radiation. In: Merrick JR, Archer M, Hickey GM, Lee MSY (eds) Evolution and biogeography of Australasian vertebrates. Auscipub, New South Wales, pp 575–646Google Scholar
  7. Archer M, Kirsch JAW (2006) The evolution and classification of marsupials. In: Armati PJ, Dickman CR, Hume ID (eds) Marsupials. Cambridge University Press, New York, pp 1–21Google Scholar
  8. Archer M, Wade M (1976) Results of the Ray E Lemley Expeditions: part 1 the Allingham Formation and a new Pliocene vertebrate fauna from northern Queensland Australia. Mem Qld Mus 17:379–398Google Scholar
  9. Archer M, Tedford RH, Rich TH (1987) The Pilkipildridae, a new family and new species of? petauroid possums (Marsupialia: Phalangerida) from the Australian Miocene. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons, Chipping Norton, New South Wales, pp 607–628Google Scholar
  10. Archer M, Arena R, Bassarova M, Black K, Brammall J, Cooke B, Creaser P, Crosby K, Gillespie A, Godthelp H, Gott M, Hand SJ, Kear B, Krikmann A, Mackness B, Muirhead J, Musser A, Myers T, Pledge N, Wang Y, Wroe S (1999) The evolutionary history and diversity of Australian mammals. Aust Mammal 21:1–45Google Scholar
  11. Asher RJ, Horovitz I, Sánchez-Villagra MR (2004) First combined cladistic analysis of marsupial mammal interrelationships. Mol Phylogenet Evol 33:240–250PubMedCrossRefGoogle Scholar
  12. Benton MJ, Ayala FJ (2003) Dating the tree of life. Science 300:1698–1700PubMedCrossRefGoogle Scholar
  13. Benton MJ, Donoghue PCJ (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24:26–53PubMedCrossRefGoogle Scholar
  14. Brammall JR (1998) A new petauroid possum from the Oligo-Miocene of Riversleigh, northwestern Queensland. Alcheringa 23:31–50CrossRefGoogle Scholar
  15. Brammall J, Archer M (1999) Living and extinct petaurids, acrobatids, tarsipedids and burramyids (Marsupialia): relationships and diversity through time. Aust Mammal 21:24–25Google Scholar
  16. Burk A, Westerman M, Kao DJ, Kavanagh JR, Springer MS (1999) An analysis of marsupial interordinal relationships based on 12S rRNA, tRNA valine, 16S rRNA, and cytochrome b sequences. J Mammal Evol 6:317–334CrossRefGoogle Scholar
  17. Case JA (1984) A new genus of Potoroinae (Marsupialia Macropodidae) from the Miocene Ngapakaldi Local Fauna, South Australia, and a definition of the Potoroinae. J Paleontol 58:1074–1086Google Scholar
  18. Case JA (1989) Antarctica: The effect of high latitude heterochroneity on the origin of the Australian marsupials. In: Crame JA (ed) Origins and evolution of the Antarctic biota. Geological Society Special Publication 47, pp 217–226Google Scholar
  19. Case JA (2001) Turnover of bandicoots in the Oligo-Miocene of South Australia. J Vertebr Paleontol Supp 21:39AGoogle Scholar
  20. Case JA, Goin FJ, Woodburne MO (2005) “South American” marsupials from the Late Cretaceous of North America and the origin of marsupial cohorts. J Mammal Evol 12:461–494CrossRefGoogle Scholar
  21. Cooke BN (2006) Kangaroos. In: Merrick JR, Archer M, Hickey GM, Lee MSY (eds) Evolution and biogeography of Australasian vertebrates. Auscipub, New South Wales, pp 647–672Google Scholar
  22. Cooke B, Kear B (1999) Evolution and diversity of kangaroos (Macropodoidea, Marsupialia). Aust Mammal 21:27–29Google Scholar
  23. Cozzuol MA, Goin F, Reyes MDL, Ranzi A (2006) The oldest species of Didelphis (Mammalia, Marsupialia, Didelphidae), from the late Miocene of Amazonia. J Mammal 87:663–667CrossRefGoogle Scholar
  24. Crochet J-Y, Sigé B (1993) Les mammifères de Chulpas (Formation Umayo, transition Crétacé-Tertiaire, Pérou): données préliminaires. Documents Lab Géol Faculté Sci Lyon 125:97–107Google Scholar
  25. Crosby K, Bassarova M, Archer M, Carbery K (2004) Fossil possums in Australasia: discovery, diversity and evolution. In: Goldingay RL, Jackson SM (ed) The biology of Australian possums and gliders. Beatty, Sydney, pp 161–176Google Scholar
  26. Czaplewski NJ, Masanaru T, Naeher, TM, Shigehara N, Setoguchi T (2003) Additional bats from the middle Miocene La Venta fauna of Colombia. Rev Acad Colomb Cienc 27:263–282Google Scholar
  27. De Queiroz A (1993) For consensus (sometimes). Syst Biol 42:368–372CrossRefGoogle Scholar
  28. Drummond AJ, Rambaut A (2003) BEAST version 14 [computer program] Available http://evolvezoooxacuk/beast Accessed January 2007
  29. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710CrossRefGoogle Scholar
  30. Edwards D, Westerman M (1995) The molecular relationships of possum and glider families as revealed by DNA–DNA hybridisations. Aust J Zool 43:231–240CrossRefGoogle Scholar
  31. Farris JS, Kallersjo M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319CrossRefGoogle Scholar
  32. Flannery T (1987) The relationships of the macropodoids (Marsupialia) and the polarity of some morphological features within the Phalangeriformes. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons, Chipping Norton, New South Wales, pp 741–748Google Scholar
  33. Flannery TF (1989) Phylogeny of the Macropodoidea; a case study in convergence. In: Grigg GC, Jarman PJ, Hume ID (eds) Kangaroos, wallabies and rat–kangaroos. Surrey Beatty and Sons, Chipping Norton, New South Wales, pp 1–46Google Scholar
  34. Godthelp H, Wroe S, Archer M (1999) A new marsupial from the early Eocene Tingamarra local Fauna of Murgon, southeastern Queensland: a prototypical Australian marsupial? J Mammal Evol 6:289–313CrossRefGoogle Scholar
  35. Goin FJ (1997) New clues for understanding Neogene marsupial radiations. In: Kay RF (ed) Vertebrate paleontology in the Neotropics: the Miocene fauna of La Venta, Colombia. Smithsonian Institution, Washington, DC, pp 187–206Google Scholar
  36. Goin FJ, Pascual R, Tejedor MF, Gelfo JN, Woodburne MO, Case JA, Reguero MA, Bond M, Lopez GM, Cione AL, Udrizar Sauthier D, Balarino L, Scasso RA, Medina FA, Ubaldon MC (2006) The earliest Tertiary therian mammal from South America. J Vertebr Paleontol 26:505–510CrossRefGoogle Scholar
  37. Gradstein FM, Ogg JG, Smith AG, 39 co-authors (2004) A geologic timescale. Cambridge University Press, CambridgeGoogle Scholar
  38. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  39. Gunson MM, Sharman GB, Thomson JA (1968) The affinities of Burramys (Marsupialia: Phalangeroidea) as revealed by its chromosomes. Aust J Sci 31:40–41Google Scholar
  40. Harding HR (1987) Interrelationships of the families of the Diprotodontia—a view based on spermatozoan ultrastructure. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons, Chipping Norton, New South Wales, pp 195–216Google Scholar
  41. Hasegawa M, Thorne JL, Kishino H (2003) Time scale of eutherian evolution estimated without assuming a constant rate of molecular evolution. Genes Genet Syst 78:267–283PubMedCrossRefGoogle Scholar
  42. Heads M (2002) Birds of paradise, vicariance biogeography and terrane tectonics in New Guinea. J Biogeog 29:261–283CrossRefGoogle Scholar
  43. Hedges SB, Kumar S (2004) Precision of molecular time estimates. Trends Gen 20:242–247CrossRefGoogle Scholar
  44. Hershkovitz P (1992) Ankle bones: the Chilean opossum Dromiciops gliroides Thomas, and marsupial phylogeny. Bonn Zool Beit 43:181–213Google Scholar
  45. Horovitz I, Sánchez-Villagra MR (2003) A morphological analysis of marsupial mammal higher-level phylogenetic relationships. Cladistics 19:181–212CrossRefGoogle Scholar
  46. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  47. Hughes RL (1965) Comparative morphology of spermatozoa from five families. Aust J Zool 13:533–543CrossRefGoogle Scholar
  48. Jansa SA, Voss RS (2005) Phylogenetic relationships of the marsupial genus Hyladelphys based on nuclear gene sequences and morphology. J Mammal 86:853–865CrossRefGoogle Scholar
  49. Johnson WE, Eizirik E, Pecon-Slattery J, Murphy WJ, Antunes A, Teeling E, O’Brien SJ (2006) The late Miocene radiation of modern Felidae: a genetic assessment. Science 311:73–77PubMedCrossRefGoogle Scholar
  50. Kavanagh JR, Burk-Herrick A, Westerman M, Springer MS (2004) Relationships among families of Diprotodontia (Marsupialia) and the phylogenetic position of the autapomorphic honey possum (Tarsipes rostratus). J Mammal Evol 11:207–222CrossRefGoogle Scholar
  51. Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004) Mammals from the age of dinosaurs: origins, evolution, and structure. Columbia University Press, New YorkGoogle Scholar
  52. Kirsch JA (1968) Prodromus of the comparative serology of Marsupialia. Nature 217:418–420PubMedCrossRefGoogle Scholar
  53. Kirsch JAW (1977) The comparative serology of Marsupialia and a classification of marsupials. Aust J Zool, Supp Ser 52:1–152Google Scholar
  54. Kirsch JAW, Palma RE (1995) DNA/DNA hybridization studies of carnivorous marsupials. V. A further estimate of relationships among opossums (Marsupialia: Didelphidae). Mammalia 59:403–425Google Scholar
  55. Kirsch JAW, Krajewski C, Springer MS, Archer M (1990) DNA–DNA hybridization studies of carnivorous marsupials. II. Relationships among dasyurids (Marsupialia: Dasyuridae). Aust J Zool 38:673–696CrossRefGoogle Scholar
  56. Kirsch JAW, Dickerman AW, Reig OA, Springer MS (1991) DNA hybridization evidence for the Australasian affinity of the American marsupial Dromiciops australis. Proc Natl Acad Sci USA 88:10465–10469PubMedCrossRefGoogle Scholar
  57. Kirsch JAW, Lapointe F-J, Springer MS (1997) DNA-hybridisation studies of marsupials and their implications for metatherian classification. Aust J Zool 45:211–280CrossRefGoogle Scholar
  58. Kishino H, 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 29:170–179PubMedCrossRefGoogle Scholar
  59. Kishino H, Thorne JL, Bruno WJ (2001) Performance of a divergence time estimation method under a probabilistic model of rate evolution. Mol Biol Evol 18:352–361PubMedGoogle Scholar
  60. Krajewski C, Young J, Buckley L, Woolley PA, Westerman M (1997) Reconstructing the evolutionary radiation of dasyurine marsupials with cytochrome b, 12S rRNA, and protamine P1 gene trees. J Mammal Evol 4:217–236CrossRefGoogle Scholar
  61. Krajewski C, Blacket MJ, Westerman M (2000) DNA sequence analysis of familial relationships among dasyuromorphian marsupials. J Mammal Evol 7:95–108CrossRefGoogle Scholar
  62. Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920PubMedCrossRefGoogle Scholar
  63. Langford RP, Wilford GE, Truswell EM, Isern AR (1995) Palaeogeographic atlas of Australia, Volume 10 Cainozoic. Australian Geological Survey Organization, CanberraGoogle Scholar
  64. Long J, Archer M, Flannery TF, Hand SJ (2002) Prehistoric mammals of Australia and New Guinea: one hundred million years of evolution. University of New South Wales Press, SydneyGoogle Scholar
  65. Luckett WP (1994) Suprafamilial relationships within Marsupialia: resolution and discordance from multidisciplinary data. J Mammal Evol 2:255–283CrossRefGoogle Scholar
  66. Luo Z-X, Ji Q, Wible JR, Yuan C-X (2003) An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302:1934–1940PubMedCrossRefGoogle Scholar
  67. Mackness BS, Whitehead PW, McNamara GC (2000) New potassium–argon basalt date in relation to the Pliocene Bluff Downs local fauna, northern Australia. Aust J Earth Sci 47:807–811CrossRefGoogle Scholar
  68. Marshall LG (1976) New didelphine marsupials from the La-Venta Fauna Miocene of Colombia South America. J Paleontol 50:402–418Google Scholar
  69. Marshall LG, de Muizon C (1988) The dawn of the age of mammals in South America. Natl Geograph Res 4:23–55Google Scholar
  70. Marshall LG, Case JA, Woodburne MO (1990) Phylogenetic relationships of the families of marsupials. In: Genoways HH (ed) Current mammalogy, Vol 2. Plenum, New York, pp 433–506Google Scholar
  71. Marshall LG, Sempere T, Butler RF (1997) Chronostratigraphy of the mammal-bearing Paleocene of South America. J South Am Earth Sci 10:49–70CrossRefGoogle Scholar
  72. McKenna MC, Bell SK (1997) Classification of mammals above the species level. Columbia University Press, New YorkGoogle Scholar
  73. Megirian D, Murray P, Schwartz L, Vonderborsch C (2004) Late Oligocene Kangaroo Well Local Fauna from the Ulta Limestone (new name), and climate of the ‘Miocene oscillation’ across central Australia. Aust J Earth Sci 51:701–741CrossRefGoogle Scholar
  74. Muizon C de, Cifelli RL (2001) A new basal “didelphoid” (Marsupialia, Mammalia) from the early Paleocene of Tiupampa (Bolivia). J Vertebr Paleontol 21:87–97CrossRefGoogle Scholar
  75. Muirhead J, Dawson L, Archer M (1997) Perameles bowensis, a new species of Perameles (Peramelemorphia: Marsupialia) from the Pliocene faunas of Bow and Wellington Caves, New South Wales. Proc Lin Soc NSW 117:163–173Google Scholar
  76. Müller J, Reisz RR (2005) Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. BioEssays 27:1069–1075PubMedCrossRefGoogle Scholar
  77. Munemasa M, Nikaido M, Donnellan S, Austin CC, Okada N, Hasegawa M (2006) Phylogenetic analysis of diprotodontian marsupials based on complete mitochondrial genomes. Genes Genet Syst 81:181–191PubMedCrossRefGoogle Scholar
  78. Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351PubMedCrossRefGoogle Scholar
  79. Murray PF, Megirian D (1992) Continuity and contrast in middle and late Miocene vertebrate communities from the Northern Territory. Beagle 9:195–218Google Scholar
  80. Myers TJ, Archer M (1997) Kuterintja ngama (Marsupialia, Ilariidae): A revised systematic analysis based on material from the late Oligocene of Riversleigh, northwestern Queensland. Mem Qld Mus 41:379–392Google Scholar
  81. Nilsson MA, Gullberg A, Spotorno AE, Arnason U, Janke A (2003) Radiation of extant marsupials after the K/T boundary: evidence from complete mitochondrial genomes. J Mol Evol 57:S3–S12PubMedCrossRefGoogle Scholar
  82. Nilsson MA, Arnason U, Spencer PBS, Janke A (2004) Marsupial relationships and a timeline for marsupial radiation in south Gondwana. Gene 340:189–196PubMedCrossRefGoogle Scholar
  83. Osborne MJ, Christidis L (2001) Molecular phylogenetics of Australo-Papuan possums and gliders (Family Petauridae). Mol Phylogenet Evol 20:211–224PubMedCrossRefGoogle Scholar
  84. Osborne MJ, Christidis L, Norman JA (2002) Molecular phylogenetics of the Diprotodontia (kangaroos, wombats, koala, possums, and allies). Mol Phylogenet Evol 25:219–228PubMedCrossRefGoogle Scholar
  85. Penny D, Hasegawa M, Waddell PJ, Hendy MD (1999) Mammalian evolution: timing and implications from using the log determinant transform for proteins of differing amino acid composition. Syst Biol 48:76–93PubMedCrossRefGoogle Scholar
  86. Phillips MJ, Lin Y-H, Harrison GL, Penny D (2001) Mitochondrial genomes of a bandicoot and a brushtail possum confirm the monophyly of australidelphian marsupials. Proc R Soc Lond B 268:1533–1538CrossRefGoogle Scholar
  87. Phillips MJ, McLenachan PA, Down C, Gibb GC, Penny D (2006) Combined mitochondrial and nuclear DNA sequences resolve the interrelations of the major Australasian marsupial radiations. Syst Biol 55:122–137PubMedCrossRefGoogle Scholar
  88. Pledge NS (1990) The upper fossil fauna of the Henschke fossil cave, Naracoorte, South Australia. Mem Queensl Mus 28:247–262Google Scholar
  89. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  90. Price GJ (2004) Fossil bandicoots (Marsupialia, Peramelidae) and environmental change during the Pleistocene on the Darling Downs, southeastern Queensland, Australia. J Syst Palaeontol 2:347–356CrossRefGoogle Scholar
  91. Prideaux G (2004) Systematics and evolution of the sthenurine kangaroos. Univ Calif Pub Geol Sci 146:i–xvii, 1-623, Berkeley, University of California PressGoogle Scholar
  92. Rambaut A (1996) Se-Al: sequence alignment editor [computer editor]. Available at http://evolvezoooxacuk/
  93. Rambaut A, Drummond AJ (2003) Tracer version 12 [computer program]. Available http://evolvezoooxacuk Accessed August 2006
  94. Reig OA (1952) Descripcion previa de nuevos ungulados y marsupiales fosiles del Plioceno y del eocuartario Argentinos 1:119–129Google Scholar
  95. Reig OA (1958) Notas para una actualizacion del conocimiento de la fauna de la formacion Chapadmala II Amphibia, Reptilia, Aves, Mammalia (Marsupialia: Didelphidae, Borhyaenidae). Acta Geol Lilloana, 2:255–283Google Scholar
  96. Reig OA, Kirsch JAW, Marshall LG (1987) Systematic relationships of the living and Neocenozoic American “opossum-like” marsupials (Suborder Didelphimorphia) with comments on the classification of these and of the Cretaceous and Paleogene New World and European metatherians. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons, Chipping Norton, New South Wales, pp 1–90Google Scholar
  97. Reisz RR, Müller J (2004) Molecular timescales and the fossil record: a paleontological perspective. Trends Gen 20:237–241CrossRefGoogle Scholar
  98. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  99. Rougier GW, Wible JR, Novacek MJ (1998) Implications of Deltatheridium specimens for early marsupial history. Nature 396:459–463PubMedCrossRefGoogle Scholar
  100. Sánchez-Villagra MR, Wible JR (2002) Patterns of evolutionary transformation in the petrosal bone and some basicranial features in marsupial mammals, with special reference to didelphids. J Zool Syst Evol Res 40:26–45CrossRefGoogle Scholar
  101. Sánchez-Villagra MR, Ladevèze S, Horovitz I, Argot C, Hooker JJ, Macrini TE, Martin T, Moore-Fay S, Muizon C de, Schmelzle T, Asher RJ (2007) Exceptionally preserved North American Paleogene metatherians: adaptations and discovery of a major gap in the opossum fossil record. Biol Letters 3:318–322CrossRefGoogle Scholar
  102. Sanderson MJ (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 19:101–109PubMedGoogle Scholar
  103. Schwartz L (2006) A new species of bandicoot from the Oligocene of Northern Australia and implications of bandicoots for correlating Australian Tertiary mammal faunas. Palaeontol 49:991–998CrossRefGoogle Scholar
  104. Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492–508PubMedCrossRefGoogle Scholar
  105. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116Google Scholar
  106. Sigé B, Archer M, Godthelp H, Hand S, Crochet J-Y (1995) Peruvian–Australian Paleogene mammal connection. Cavep’s 95, Fifth Conference on Australian Vertebrate Evolution, Palaeontology and Systematics, Canberra, Programme and Abstracts, 2Google Scholar
  107. Sigé B, Sempere T, Butler RF, Marshall LG, Crochet J-Y (2004) Age and stratigraphic reassessment of the fossil-bearing Laguna Umayo red mudstone unit, SE Peru, from regional stratigraphy, fossil record, and paleomagnetism. Geobios 37:771–794CrossRefGoogle Scholar
  108. Simpson GG (1974) Notes on Didelphidae (Mammalia, Marsupialia) from the Huayquerian (Pliocene) of Argentina. Am Mus Novitates 2559:1–15Google Scholar
  109. Smith AB, Pisani D, Mackenzie-Dodds JA, Stockley B, Webster BL, Littlewood TJ (2006) Testing the molecular clock: molecular and paleontological estimates of divergence times in the Echinoidea (Echinodermata). Mol Biol Evol 23:1832–1851PubMedCrossRefGoogle Scholar
  110. Springer MS (1997) Molecular clocks and the timing of the placental and marsupial radiations in relation to the Cretaceous–Tertiary boundary. J Mammal Evol 4:285–302CrossRefGoogle Scholar
  111. Springer MS, Kirsch JAW (1991) DNA hybridization, the compression effect, and the radiation of diprotodontian marsupials. Syst Zool 40:131–151CrossRefGoogle Scholar
  112. Springer MS, Woodburne MO (1989) The distribution of some basicranial characters within the Marsupialia and a phylogeny of the Phalangeriformes. J Vertebr Paleontol 9:210–221CrossRefGoogle Scholar
  113. Springer MS, Kirsch JAW, Case JA (1997a) The chronicle of marsupial evolution. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiation. Cambridge University Press, New York, pp 129–161Google Scholar
  114. Springer MS, Burk A, Kavanagh JR, Waddell VG, Stanhope MJ (1997b) The interphotoreceptor retinoid binding protein gene in therian mammals: implications for higher level relationships and evidence for loss of function in the marsupial mole. Proc Natl Acad Sci USA 94:13754–13759PubMedCrossRefGoogle Scholar
  115. Springer MS, Westerman M, Kavanagh JR, Burk A, Woodburne MO, Kao DJ, Krajewski C (1998) The origin of the Australasian marsupial fauna and the phylogenetic affinities of the enigmatic monito del monte and marsupial mole. Proc R Soc Lond B 265:2381–2386CrossRefGoogle Scholar
  116. Steiner C, Tilak M, Douzery JP, Catzeflis FM (2005) New DNA data from a transthyretin nuclear intron suggest an Oligocene to Miocene diversification of living South America opossums (Marsupialia: Didelphidae). Mol Phylogenet Evol 35:363–379PubMedCrossRefGoogle Scholar
  117. Swofford DL (2002) PAUP* Phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  118. Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic inference. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics, 2nd edn. Sinauer, Sunderland, MA, pp 407–514Google Scholar
  119. Szalay FS (1982) A new appraisal of marsupial phylogeny and classification. In: Archer M (ed) Carnivorous marsupials. Royal Zoological Society of New South Wales, Sydney, pp 621–640Google Scholar
  120. Szalay FS (1994) Evolutionary history of the marsupials and an analysis of osteological characters. Cambridge University Press, New YorkGoogle Scholar
  121. Szalay FS, Sargis EJ (2001) Model-based analysis of postcranial osteology of marsupials from the Palaeocene of Itaborai (Brazil) and the phylogenetics and biogeography of Metatheria. Geodiversitas 23:139–302Google Scholar
  122. Tedford RH, Kemp NR (1998) Oligocene marsupials of the Geilston Bay local fauna, Tasmania. Am Mus Novitates 3244:1–22Google Scholar
  123. Teeling EC, Madsen O, Van Den Bussche RA, de Jong WW, Stanhope MJ, Springer MS (2002) Microbat paraphyly and the convergent evolution of a key innovation in Old World rhinolophoid microbats. Proc Natl Acad Sci USA 99:1431–1436PubMedCrossRefGoogle Scholar
  124. Teeling EC, Springer MS, Madsen O, Bates P, O’Brien SJ, Murphy WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584PubMedCrossRefGoogle Scholar
  125. Temple-Smith PD (1987) Sperm structure and marsupial phylogeny. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons, Chipping Norton, New South Wales, pp 171–193Google Scholar
  126. Thorne JL, Kishino H (2002) Divergence time and evolutionary rate estimation with multilocus data. Syst Biol 51:689–702PubMedCrossRefGoogle Scholar
  127. Thorne JL, Kishino H, Painter IS (1998) Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 15:1647–1657PubMedGoogle Scholar
  128. Turnbull WD, Lundelius EL Jr, Archer M (2003) Dasyurids, perameloids, phalangeroids, and vombatoids from the early Pliocene Hamilton fauna, Victoria, Australia. Bull Am Mus Nat Hist 279:513–540CrossRefGoogle Scholar
  129. Warburton NM (2003) Functional morphology and evolution of marsupial moles (Marsupialia; Notoryctemorphia). Thesis, The University of Western AustraliaGoogle Scholar
  130. Westerman M, Springer MS, Dixon J, Krajewski C (1999) Molecular relationships of the extinct pig-footed bandicoot Chaeropus ecaudatus (Marsupialia: Perameloidea) using 12S rRNA sequences. J Mammal Evol 6:271–288CrossRefGoogle Scholar
  131. Westerman M, Springer MS, Krajewski C (2001) Molecular relationships of the New Guinean bandicoot genera Microperoryctes and Echymipera (Marsupialia:Peramelina). J Mammal Evol 8:93–105CrossRefGoogle Scholar
  132. White ME (1994) After the greening: the browning of Australia. Kangaroo, New South WalesGoogle Scholar
  133. Wilson DE, Reeder DM (2005) Mammal species of the world: a taxonomic and geographic reference. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  134. Winge H (1941) The inter-relationships of the mammalian genera, Vol 1. Monotremata, Marsupialia, Insectivora, Chiroptera, Edentata. CA Reitzels Forlag, CopenhagenGoogle Scholar
  135. Woodburne MO (1984) Families of marsupials: relationships, evolution, and biogeography. In: Broadhead TW (ed) Mammals: notes for a short course. Univ Tenn Dept Geol Sci Stud Geol 8, pp 48–71Google Scholar
  136. Woodburne MO, Case JA (1996) Dispersal, vicariance, and the Late Cretaceous to early Tertiary land mammal biogeography from South America to Australia. J Mammal Evol 3:121–161CrossRefGoogle Scholar
  137. Woodburne MO, Tedford RH, Archer M, Turnbull WD, Plane MD, Lundelius EL Jr (1985) Biochronology of the continental mammal record of Australia and New Guinea. Spec Publ S Aust Dept Mines Energy 5:347–364Google Scholar
  138. Woodburne MO, Tedford RH, Archer M (1987) New Miocene pseudocheirids (Pseudocheiridae: Marsupialia) from South Australia. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons, Chipping Norton, New South Wales, pp 639–679Google Scholar
  139. Woodburne MO, MacFadden BJ, Case JA, Springer MS, Pledge NS, Power JD, Woodburne JM, Springer KB (1993) Land mammal biostratigraphy and magnetostratigraphy of the Etadunna Formation (late Oligocene) of South Australia. J Vertebr Paleontol 13:483–515CrossRefGoogle Scholar
  140. Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28:360–385PubMedCrossRefGoogle Scholar
  141. Wroe S (1998) The geologically oldest dasyurid, from the Miocene of Riversleigh, north-west Queensland. Palaeontol 42:501–527CrossRefGoogle Scholar
  142. Wroe S (2003) Australian marsupial carnivores: recent advances in palaeontology. In: Jones M, Dickerman C, Archer M (eds) Predators with pouches: the biology of marsupial carnivores. CSIRO, Collingwood, Australia, pp 102–123Google Scholar
  143. Wroe S, Mackness BS (2000) Additional material of Dasyurus dunmalli from the Pliocene Chinchilla Local Fauna of Queensland and its phylogenetic implications. Mem Queensl Mus 45:641–645Google Scholar
  144. Wroe S, Ebach M, Ahyong S, Muizon C de, Muirhead J (2000) Cladistic analysis of dasyuromorphian (Marsupialia) phylogeny using cranial and dental characters. J Mammal 81:1008–1024CrossRefGoogle Scholar
  145. Yang Z, Rannala B (2006) Bayesian estimation of species divergence times under a molecular clock using multiple calibrations with soft bounds. Mol Biol Evol 23:212–226PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of BiologyUniversity of CaliforniaRiversideUSA
  2. 2.Department of GeneticsLa Trobe UniversityBundooraAustralia
  3. 3.College of Science Health and EngineeringEastern Washington UniversityCheneyUSA

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