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

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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.

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References

  • 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 71:424–436

    Google Scholar 

  • Adam P (1999) Australian rainforests. Oxford University Press, Oxford

    Google Scholar 

  • 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 28:186–196

    Article  PubMed  CAS  Google Scholar 

  • 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–xxii

    Google Scholar 

  • 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. 397–443

    Google Scholar 

  • 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 575–646

    Google Scholar 

  • 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 1–21

    Google Scholar 

  • 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 17:379–398

    Google Scholar 

  • 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 607–628

    Google Scholar 

  • 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 21:1–45

    Google Scholar 

  • Asher RJ, Horovitz I, Sánchez-Villagra MR (2004) First combined cladistic analysis of marsupial mammal interrelationships. Mol Phylogenet Evol 33:240–250

    Article  PubMed  CAS  Google Scholar 

  • Benton MJ, Ayala FJ (2003) Dating the tree of life. Science 300:1698–1700

    Article  PubMed  CAS  Google Scholar 

  • Benton MJ, Donoghue PCJ (2007) Paleontological evidence to date the tree of life. Mol Biol Evol 24:26–53

    Article  PubMed  CAS  Google Scholar 

  • Brammall JR (1998) A new petauroid possum from the Oligo-Miocene of Riversleigh, northwestern Queensland. Alcheringa 23:31–50

    Article  Google Scholar 

  • Brammall J, Archer M (1999) Living and extinct petaurids, acrobatids, tarsipedids and burramyids (Marsupialia): relationships and diversity through time. Aust Mammal 21:24–25

    Google Scholar 

  • 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 6:317–334

    Article  Google Scholar 

  • 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 58:1074–1086

    Google Scholar 

  • 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 217–226

  • Case JA (2001) Turnover of bandicoots in the Oligo-Miocene of South Australia. J Vertebr Paleontol Supp 21:39A

    Google Scholar 

  • 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 12:461–494

    Article  Google Scholar 

  • 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 647–672

    Google Scholar 

  • Cooke B, Kear B (1999) Evolution and diversity of kangaroos (Macropodoidea, Marsupialia). Aust Mammal 21:27–29

    Google Scholar 

  • 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 87:663–667

    Article  Google Scholar 

  • Crochet J-Y, Sigé B (1993) Les mammifères de Chulpas (Formation Umayo, transition Crétacé-Tertiaire, Pérou): données préliminaires. Documents Lab Géol Faculté Sci Lyon 125:97–107

    Google Scholar 

  • 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 161–176

    Google Scholar 

  • 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 27:263–282

    Google Scholar 

  • De Queiroz A (1993) For consensus (sometimes). Syst Biol 42:368–372

    Article  Google Scholar 

  • Drummond AJ, Rambaut A (2003) BEAST version 14 [computer program] Available http://evolvezoooxacuk/beast Accessed January 2007

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710

    Article  CAS  Google Scholar 

  • Edwards D, Westerman M (1995) The molecular relationships of possum and glider families as revealed by DNA–DNA hybridisations. Aust J Zool 43:231–240

    Article  Google Scholar 

  • Farris JS, Kallersjo M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • 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 741–748

    Google Scholar 

  • 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 1–46

    Google Scholar 

  • 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 6:289–313

    Article  Google Scholar 

  • 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 187–206

    Google Scholar 

  • 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 26:505–510

    Article  Google Scholar 

  • Gradstein FM, Ogg JG, Smith AG, 39 co-authors (2004) A geologic timescale. Cambridge University Press, Cambridge

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Gunson MM, Sharman GB, Thomson JA (1968) The affinities of Burramys (Marsupialia: Phalangeroidea) as revealed by its chromosomes. Aust J Sci 31:40–41

    Google Scholar 

  • 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 195–216

    Google Scholar 

  • Hasegawa M, Thorne JL, Kishino H (2003) Time scale of eutherian evolution estimated without assuming a constant rate of molecular evolution. Genes Genet Syst 78:267–283

    Article  PubMed  CAS  Google Scholar 

  • Heads M (2002) Birds of paradise, vicariance biogeography and terrane tectonics in New Guinea. J Biogeog 29:261–283

    Article  Google Scholar 

  • Hedges SB, Kumar S (2004) Precision of molecular time estimates. Trends Gen 20:242–247

    Article  CAS  Google Scholar 

  • Hershkovitz P (1992) Ankle bones: the Chilean opossum Dromiciops gliroides Thomas, and marsupial phylogeny. Bonn Zool Beit 43:181–213

    Google Scholar 

  • Horovitz I, Sánchez-Villagra MR (2003) A morphological analysis of marsupial mammal higher-level phylogenetic relationships. Cladistics 19:181–212

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Hughes RL (1965) Comparative morphology of spermatozoa from five families. Aust J Zool 13:533–543

    Article  Google Scholar 

  • Jansa SA, Voss RS (2005) Phylogenetic relationships of the marsupial genus Hyladelphys based on nuclear gene sequences and morphology. J Mammal 86:853–865

    Article  Google Scholar 

  • 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 311:73–77

    Article  PubMed  CAS  Google Scholar 

  • 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 11:207–222

    Article  Google Scholar 

  • Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004) Mammals from the age of dinosaurs: origins, evolution, and structure. Columbia University Press, New York

    Google Scholar 

  • Kirsch JA (1968) Prodromus of the comparative serology of Marsupialia. Nature 217:418–420

    Article  PubMed  CAS  Google Scholar 

  • Kirsch JAW (1977) The comparative serology of Marsupialia and a classification of marsupials. Aust J Zool, Supp Ser 52:1–152

    Google Scholar 

  • Kirsch JAW, Palma RE (1995) DNA/DNA hybridization studies of carnivorous marsupials. V. A further estimate of relationships among opossums (Marsupialia: Didelphidae). Mammalia 59:403–425

    Google Scholar 

  • 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 38:673–696

    Article  Google Scholar 

  • 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 88:10465–10469

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 29:170–179

    Article  PubMed  CAS  Google Scholar 

  • Kishino H, Thorne JL, Bruno WJ (2001) Performance of a divergence time estimation method under a probabilistic model of rate evolution. Mol Biol Evol 18:352–361

    PubMed  CAS  Google Scholar 

  • 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 4:217–236

    Article  Google Scholar 

  • Krajewski C, Blacket MJ, Westerman M (2000) DNA sequence analysis of familial relationships among dasyuromorphian marsupials. J Mammal Evol 7:95–108

    Article  Google Scholar 

  • Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920

    Article  PubMed  CAS  Google Scholar 

  • Langford RP, Wilford GE, Truswell EM, Isern AR (1995) Palaeogeographic atlas of Australia, Volume 10 Cainozoic. Australian Geological Survey Organization, Canberra

    Google Scholar 

  • 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, Sydney

    Google Scholar 

  • Luckett WP (1994) Suprafamilial relationships within Marsupialia: resolution and discordance from multidisciplinary data. J Mammal Evol 2:255–283

    Article  Google Scholar 

  • Luo Z-X, Ji Q, Wible JR, Yuan C-X (2003) An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302:1934–1940

    Article  PubMed  CAS  Google Scholar 

  • 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 47:807–811

    Article  Google Scholar 

  • Marshall LG (1976) New didelphine marsupials from the La-Venta Fauna Miocene of Colombia South America. J Paleontol 50:402–418

    Google Scholar 

  • Marshall LG, de Muizon C (1988) The dawn of the age of mammals in South America. Natl Geograph Res 4:23–55

    Google Scholar 

  • 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 433–506

    Google Scholar 

  • Marshall LG, Sempere T, Butler RF (1997) Chronostratigraphy of the mammal-bearing Paleocene of South America. J South Am Earth Sci 10:49–70

    Article  Google Scholar 

  • McKenna MC, Bell SK (1997) Classification of mammals above the species level. Columbia University Press, New York

    Google Scholar 

  • 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 51:701–741

    Article  Google Scholar 

  • Muizon C de, Cifelli RL (2001) A new basal “didelphoid” (Marsupialia, Mammalia) from the early Paleocene of Tiupampa (Bolivia). J Vertebr Paleontol 21:87–97

    Article  Google Scholar 

  • 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 117:163–173

    Google Scholar 

  • Müller J, Reisz RR (2005) Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. BioEssays 27:1069–1075

    Article  PubMed  Google Scholar 

  • 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 81:181–191

    Article  PubMed  CAS  Google Scholar 

  • 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 294:2348–2351

    Article  PubMed  CAS  Google Scholar 

  • Murray PF, Megirian D (1992) Continuity and contrast in middle and late Miocene vertebrate communities from the Northern Territory. Beagle 9:195–218

    Google Scholar 

  • 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 41:379–392

    Google Scholar 

  • 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–S12

    Article  PubMed  CAS  Google Scholar 

  • Nilsson MA, Arnason U, Spencer PBS, Janke A (2004) Marsupial relationships and a timeline for marsupial radiation in south Gondwana. Gene 340:189–196

    Article  PubMed  CAS  Google Scholar 

  • Osborne MJ, Christidis L (2001) Molecular phylogenetics of Australo-Papuan possums and gliders (Family Petauridae). Mol Phylogenet Evol 20:211–224

    Article  PubMed  CAS  Google Scholar 

  • Osborne MJ, Christidis L, Norman JA (2002) Molecular phylogenetics of the Diprotodontia (kangaroos, wombats, koala, possums, and allies). Mol Phylogenet Evol 25:219–228

    Article  PubMed  CAS  Google Scholar 

  • 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 48:76–93

    Article  PubMed  CAS  Google Scholar 

  • 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 268:1533–1538

    Article  CAS  Google Scholar 

  • 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 55:122–137

    Article  PubMed  Google Scholar 

  • Pledge NS (1990) The upper fossil fauna of the Henschke fossil cave, Naracoorte, South Australia. Mem Queensl Mus 28:247–262

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Price GJ (2004) Fossil bandicoots (Marsupialia, Peramelidae) and environmental change during the Pleistocene on the Darling Downs, southeastern Queensland, Australia. J Syst Palaeontol 2:347–356

    Article  Google Scholar 

  • Prideaux G (2004) Systematics and evolution of the sthenurine kangaroos. Univ Calif Pub Geol Sci 146:i–xvii, 1-623, Berkeley, University of California Press

  • Rambaut A (1996) Se-Al: sequence alignment editor [computer editor]. Available at http://evolvezoooxacuk/

  • Rambaut A, Drummond AJ (2003) Tracer version 12 [computer program]. Available http://evolvezoooxacuk Accessed August 2006

  • Reig OA (1952) Descripcion previa de nuevos ungulados y marsupiales fosiles del Plioceno y del eocuartario Argentinos 1:119–129

  • 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, 2:255–283

    Google Scholar 

  • 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 1–90

    Google Scholar 

  • Reisz RR, Müller J (2004) Molecular timescales and the fossil record: a paleontological perspective. Trends Gen 20:237–241

    Article  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rougier GW, Wible JR, Novacek MJ (1998) Implications of Deltatheridium specimens for early marsupial history. Nature 396:459–463

    Article  PubMed  CAS  Google Scholar 

  • 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 40:26–45

    Article  Google Scholar 

  • 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 3:318–322

    Article  Google Scholar 

  • Sanderson MJ (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 19:101–109

    PubMed  CAS  Google Scholar 

  • 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 49:991–998

    Article  Google Scholar 

  • Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492–508

    Article  PubMed  Google Scholar 

  • Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116

    CAS  Google Scholar 

  • 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, 2

  • 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 37:771–794

    Article  Google Scholar 

  • Simpson GG (1974) Notes on Didelphidae (Mammalia, Marsupialia) from the Huayquerian (Pliocene) of Argentina. Am Mus Novitates 2559:1–15

    Google Scholar 

  • 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 23:1832–1851

    Article  PubMed  CAS  Google Scholar 

  • Springer MS (1997) Molecular clocks and the timing of the placental and marsupial radiations in relation to the Cretaceous–Tertiary boundary. J Mammal Evol 4:285–302

    Article  Google Scholar 

  • Springer MS, Kirsch JAW (1991) DNA hybridization, the compression effect, and the radiation of diprotodontian marsupials. Syst Zool 40:131–151

    Article  Google Scholar 

  • Springer MS, Woodburne MO (1989) The distribution of some basicranial characters within the Marsupialia and a phylogeny of the Phalangeriformes. J Vertebr Paleontol 9:210–221

    Article  Google Scholar 

  • 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 129–161

    Google Scholar 

  • 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 94:13754–13759

    Article  PubMed  CAS  Google Scholar 

  • 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 265:2381–2386

    Article  CAS  Google Scholar 

  • 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 35:363–379

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2002) PAUP* Phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer Associates, Sunderland, Massachusetts

  • 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 407–514

    Google Scholar 

  • 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 621–640

    Google Scholar 

  • Szalay FS (1994) Evolutionary history of the marsupials and an analysis of osteological characters. Cambridge University Press, New York

    Google Scholar 

  • 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 23:139–302

    Google Scholar 

  • Tedford RH, Kemp NR (1998) Oligocene marsupials of the Geilston Bay local fauna, Tasmania. Am Mus Novitates 3244:1–22

    Google Scholar 

  • 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 99:1431–1436

    Article  PubMed  CAS  Google Scholar 

  • 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 307:580–584

    Article  PubMed  CAS  Google Scholar 

  • 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 171–193

    Google Scholar 

  • Thorne JL, Kishino H (2002) Divergence time and evolutionary rate estimation with multilocus data. Syst Biol 51:689–702

    Article  PubMed  Google Scholar 

  • Thorne JL, Kishino H, Painter IS (1998) Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 15:1647–1657

    PubMed  CAS  Google Scholar 

  • 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 279:513–540

    Article  Google Scholar 

  • Warburton NM (2003) Functional morphology and evolution of marsupial moles (Marsupialia; Notoryctemorphia). Thesis, The University of Western Australia

  • 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 6:271–288

    Article  Google Scholar 

  • Westerman M, Springer MS, Krajewski C (2001) Molecular relationships of the New Guinean bandicoot genera Microperoryctes and Echymipera (Marsupialia:Peramelina). J Mammal Evol 8:93–105

    Article  Google Scholar 

  • White ME (1994) After the greening: the browning of Australia. Kangaroo, New South Wales

    Google Scholar 

  • Wilson DE, Reeder DM (2005) Mammal species of the world: a taxonomic and geographic reference. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Winge H (1941) The inter-relationships of the mammalian genera, Vol 1. Monotremata, Marsupialia, Insectivora, Chiroptera, Edentata. CA Reitzels Forlag, Copenhagen

  • 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 48–71

  • 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 3:121–161

    Article  Google Scholar 

  • 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 5:347–364

    Google Scholar 

  • 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 639–679

    Google Scholar 

  • 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 13:483–515

    Article  Google Scholar 

  • Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28:360–385

    Article  PubMed  CAS  Google Scholar 

  • Wroe S (1998) The geologically oldest dasyurid, from the Miocene of Riversleigh, north-west Queensland. Palaeontol 42:501–527

    Article  Google Scholar 

  • 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 102–123

    Google Scholar 

  • 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 45:641–645

    Google Scholar 

  • 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 81:1008–1024

    Article  Google Scholar 

  • Yang Z, Rannala B (2006) Bayesian estimation of species divergence times under a molecular clock using multiple calibrations with soft bounds. Mol Biol Evol 23:212–226

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We dedicate this paper to the memory of our friend and colleague John A. W. Kirsch. MSS acknowledges support from NSF.

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Authors and Affiliations

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

    Robert W. Meredith & Mark S. Springer

  2. Department of Genetics, La Trobe University, Bundoora, Victoria, 3083, Australia

    Michael Westerman

  3. College of Science Health and Engineering, Eastern Washington University, Cheney, WA, 99004, USA

    Judd A. Case

Authors
  1. Robert W. Meredith
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  2. Michael Westerman
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  3. Judd A. Case
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  4. Mark S. Springer
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Correspondence to Robert W. Meredith or Mark S. Springer.

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Meredith, R.W., Westerman, M., Case, J.A. et al. A Phylogeny and Timescale for Marsupial Evolution Based on Sequences for Five Nuclear Genes. J Mammal Evol 15, 1–36 (2008). https://doi.org/10.1007/s10914-007-9062-6

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