Journal of Mammalian Evolution

, Volume 20, Issue 4, pp 279–290 | Cite as

Why are There Fewer Marsupials than Placentals? On the Relevance of Geography and Physiology to Evolutionary Patterns of Mammalian Diversity and Disparity



Placental mammals occupy a larger morphospace and are taxonomically more diverse than marsupials by an order of magnitude, as shown by quantitative and phylogenetic studies of several character complexes and clades. Many have suggested that life history acts as a constraint on the evolution of marsupial morphology. However, the frequent circumvention of constraints suggests that the pattern of morphospace occupation in marsupials is more a reflection of lack of ecological opportunity than one of biases in the production of variants during development. Features of marsupial physiology are a potential source of biases in the evolution of the group; these could be coupled with past macroevolutionary patterns that followed conditions imposed by global temperature changes. This is evident at the K/Pg boundary and at the Eocene/Oligocene boundary. The geographic pattern of taxonomic and morphological diversity in placental clades mirrors that of extant placentals as a whole versus marsupials: placentals of northern origin are more diverse those of southern one and include the clades that are outliers in taxonomic (rodents and bats) and ecomorphological (whales and bats) richness.


Evolution Extinction Paleontology Phylogeny Development Constraint Limbs 


  1. Antoine PO, Marivaux L, Croft DA, Billet G, Ganerød M, Jaramillo C, Martin T, Orliac MJ, Tejada J, Altamirano AJ, Duranthon F, Fanjat G, Rousse S, Gismondi RS (2012) Middle Eocene rodents from Peruvian Amazonia reveal the pattern and timing of caviomorph origins and biogeography. Proc Roy Soc B 279:1319–1326CrossRefGoogle Scholar
  2. Archer M (1978) The nature of the molar-premolar boundary in marsupials and a reinterpretation of the homology of marsupial cheekteeth. Mem Queensland Museum 18:157–164Google Scholar
  3. Archer M, Hand S, Godthelp H (2001) Australia’s Lost World: Prehistoric Animals of Riversleigh. Indiana University Press, BloomingtonGoogle Scholar
  4. Archibald JD (2011) Extinction and Radiation: How the Fall of the Dinosaurs Led to the Rise of The Mammals. Johns Hopkins University Press, BaltimoreGoogle Scholar
  5. Arena DA, M Archer, H Godthelp, SJ Hand, S Hocknull (2012) Hammer-toothed ‘marsupial skinks’ from the Australian Cenozoic. Proc Roy Soc B 278: 3529–3533CrossRefGoogle Scholar
  6. Arthur W (2011) Evolution. Wiley-Blackwell, ChichesterGoogle Scholar
  7. Asher RJ, Lin KH, Kardjilov N, Hautier LJ (2011) Variability and constraint in the mammalian vertebral column. J Evol Biol 24:1080–1090Google Scholar
  8. Beard C (2002) East of Eden at the Paleocene/Eocene Boundary. Science 295:2028–2029PubMedCrossRefGoogle Scholar
  9. Beck RMD (2008) A dated phylogeny of marsupials using a molecular supermatrix and multiple fossil constraints. J Mammal 89:75–189CrossRefGoogle Scholar
  10. Beck RMD (2012) An ‘ameridelphian’ marsupial from the early Eocene of Australia supports a complex model of Southern Hemisphere marsupial biogeography. Naturwissenschaften 99:715–729Google Scholar
  11. Bennett CV, Goswami A (2011) Does reproductive strategy drive limb integration in marsupials and monotremes? Mammal Biol 76:79–83Google Scholar
  12. Benton MJ (2009) The Red Queen and the Court Jester: species diversity and the role of biotic and abiotic factors through time. Science 323:728–32.PubMedCrossRefGoogle Scholar
  13. Bergqvist LP, Lima Moreira A, Ribeiro Pinto D (2006) Bacia de São José de Itaboraí. 75 Anos de História e Ciência. Serviço Geológico do Brasil, Rio de JaneiroGoogle Scholar
  14. Bickelmann C, Mitgutsch C, Richardson MK, Jiménez R, de Bakker MAG, Sánchez-Villagra MR (2012) Transcriptional heterochrony in talpid mole autopods. Evo-Devo (BMC) 3:16Google Scholar
  15. Bininda-Emonds ORP, Jeffery JE, Sánchez-Villagra MR, Hanken J, Colbert M, Pieau C, Selwood L, Cate C t, Raynaud A, Osabutey CK, Richardson MK (2007) Forelimb-hind limb developmental timing across tetrapods. BMC Evol. Biol 7:182Google Scholar
  16. Black KH, Archer M, Hand SJ, Godthelp H (2012) The rise of Australian marsupials: a synopsis of biostratigraphic, phylogenetic, palaeoecologic and palaeobiogeographic understanding. In: Talent JA (ed) Earth and Life: Global Biodiversity, Extinction Intervals and Biogeographic Perturbations Through Time. Springer, Dordrecht, pp 983–1078CrossRefGoogle Scholar
  17. Bloch JI, Rose KD, Gingerich PD (1998) New species of Batodonoides (Lipotyphla, Geolabididae) from the early Eocene of Wyoming: smallest known mammal? J Mammal 79:804–827CrossRefGoogle Scholar
  18. Burghardt GM (2005) The Genesis of Animal Play: Testing the Limits. Wiley, ChichesterGoogle Scholar
  19. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277359PubMedCrossRefGoogle Scholar
  20. Case JA, Goin FJ, Woodburne MO (2004) “South American” marsupials from the Late Cretaceous of North America and the origin of marsupial cohorts. J Mammal Evol 11:223255CrossRefGoogle Scholar
  21. Ceballos G, Ehrlich PR (2009) Discoveries of new mammal species and their implications for conservation and ecosystem services. Proc Natl Acad Sci USA 106:3841–3846PubMedCentralPubMedCrossRefGoogle Scholar
  22. Chornogubsky L, Goin FJ, Reguero M (2009) A reassessment of Antarctic polydolopid marsupials (middle Eocene, La Meseta Formation). Antarctic Sci 21:285–297CrossRefGoogle Scholar
  23. Cifelli RL, Muizon C de (1998) Tooth eruption and replacement pattern in early marsupials. Compt Rend de l’Acad Sci Série II Sci Terr Planèt 326:215–220Google Scholar
  24. Coetzee JM (1986) Foe. Penguin Books, UKGoogle Scholar
  25. Cooper J, Steppan SJ (2010) Developmental constraint on the evolution of marsupial forelimb morphology. Austral J Zool 58:1–15CrossRefGoogle Scholar
  26. Dawson TJ, Mifsud B, Raad MC, Webster KN (2004) Aerobic characteristics of red kangaroo skeletal muscles: is a high aerobic capacity matched by muscle mitochondrial and capillary morphology as in placental mammals? J Exp Biol 207:2811–2821PubMedCrossRefGoogle Scholar
  27. Dickman C (2007) A Fragile Balance. The Extraordinary Story of Australian Marsupials. University of Chicago Press, ChicagoGoogle Scholar
  28. Dos Reis M, Inoue J, Hasegawa M, Asher RJ, Donoghue PCJ, Yang Z (2012) Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc Roy Soc B 279:3491–3500CrossRefGoogle Scholar
  29. Forasiepi AM, Carlini AA (2010) A new thylacosmilid (Mammalia, Metatheria, Sparassodonta) from the Miocene of Patagonia, Argentina. Zootaxa 2552:55–68Google Scholar
  30. Formoso AE, Sauthier Udrizar DE, Teta P, Pardiñas UFJ (2011) Dense-sampling reveals a complex distributional pattern between the southernmost marsupials Lestodelphys and Thylamys in Patagonia, Argentina. Mammalia 75:371–379CrossRefGoogle Scholar
  31. Fortelius M, Kappelman J (1993) The largest land mammal ever imagined. Zool J Linn Soc 108:85–101Google Scholar
  32. Fox RC, Naylor BG (2006) Stagodontid marsupials from the Late Cretaceous of Canada and their systematic and functional implications. Acta Palaeontol Pol 51:13–36Google Scholar
  33. Frankenberg F, Dopheide B, Shaw G, Renfree MB (2011) A novel MSMB-related microprotein in the postovulatory egg coats of marsupials. BMC Evol Biol 11:373PubMedCentralPubMedCrossRefGoogle Scholar
  34. Fröbisch NB (2008) Ossification patterns in the tetrapod limb - conservation and divergence from morphogenetic events. Biol Rev 83:571–600PubMedCrossRefGoogle Scholar
  35. Gavrilets S, Losos JB (2009) Adaptive radiation: contrasting theory with data. Science 323:732–737PubMedCrossRefGoogle Scholar
  36. Geiser F (1994) Hibernation and daily torpor in marsupials: a review. Austral J Zool 42:1–16CrossRefGoogle Scholar
  37. Gemmel RT, Veitch C, Nelson J (2002) Birth in marsupials. Comp Bioch Physiol 131:621–630CrossRefGoogle Scholar
  38. Godthelp H, Archer M, Cifelli RL, Hand SJ, Gilkeson CF (1992) Earliest known Australian Tertiary mammal fauna. Nature 356:514–516CrossRefGoogle Scholar
  39. Goin FJ, Abello MA, Chornogubsky L (2010) Middle Tertiary marsupials from central Patagonia (early Oligocene of Gran Barranca): Understanding South America’s Grande Coupure. In: Madden RH, AA Carlini, MG Vucetich, RF Kay (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 36–47Google Scholar
  40. Goin FJ, Case JA, Woodburne MO, Vizcaíno SF, Reguero MA (1999) New discoveries of “opposum-like” marsupials from Antarctica (Seymour Island, medial Eocene). J Mammal Evol 6:335–365CrossRefGoogle Scholar
  41. Goin FJ, Zimicz AN, Forasiepi AM, Chornogubsky L, Abello MA (2012) The rise and fall of South American metatherians: contexts, adaptations, radiations, and extinctions. In: Rosenberger AL, MF Tejedor (eds) Origins and Evolution of Cenozoic South American Mammals. Springer Verlag, BerlinGoogle Scholar
  42. Gordon G, Hulbert AJ (1989) Fauna of Australia: Mammalia. Australian Government Publishing Service, CanberraGoogle Scholar
  43. Goswami A (2012) A dating success story: genomes and fossils converge on placental mammal origins. EvoDevo 3:18PubMedCentralPubMedCrossRefGoogle Scholar
  44. Goswami A, Milne N, Wroe S (2011) Biting through constraints: cranial morphology, disparity, and convergence across living and fossil carnivorous mammals. Proc Roy Soc B 278:1831–1839CrossRefGoogle Scholar
  45. Goswami A, Polly PD, Mock O, Sánchez-Villagra MR (2012) Shape, variance and integration during craniogenesis: contrasting marsupial and placental mammals. J Evol Biol 25:862–872PubMedCrossRefGoogle Scholar
  46. Goswami A, Weisbecker V, Sánchez-Villagra MR (2009) Developmental modularity and the marsupial-placental dichotomy. J Exp Zool B Mol Dev Evol 312B:186–195PubMedCrossRefGoogle Scholar
  47. Gould SJ (1977) Ontogeny and Phylogeny. Belknap Press, CambridgeGoogle Scholar
  48. Gould SJ (1980) The Panda’s Thumb. W.W. Norton and Company, New YorkGoogle Scholar
  49. Hamrick MW (1999) Development of epiphyseal structure and function in Didelphis virginiana (Marsupiala, Didelphidae). J Morphol 239:283–296CrossRefGoogle Scholar
  50. Hand SJ, Novacek MJ, Godthelp H, Archer M (1994) First Eocene bat from Australia. J Vertebr Paleontol 14:375–81CrossRefGoogle Scholar
  51. Hand SJ, Weisbecker V, Beck RM, Archer M, Godthelp H, Tennyson AJ, Worthy TH (2009) Bats that walk: a new evolutionary hypothesis for the terrestrial behaviour of New Zealand’s endemic mystacinids. BMC Evol Biol 9:169Google Scholar
  52. Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ (2010) Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proc Natl Acad Sci USA 107:18903–18908PubMedCentralPubMedCrossRefGoogle Scholar
  53. Hayward JS, Lisson PA (1992) Evolution of brown fat: its absence in marsupials and monotremes. Can J Zool 70:171–179CrossRefGoogle Scholar
  54. Holloway JC, Geiser F (2001) Seasonal changes in the thermoenergetics of the marsupial sugar glider, Petaurus breviceps. J Comp Physiol B 171:643–650PubMedCrossRefGoogle Scholar
  55. Hooker JJ, Sánchez-Villagra MR, Goin FJ, Simons EL, Attia Y, Seiffert ER (2008) The origin of Afro-Arabian ‘didelphimorph’ marsupials. Palaeontology 51:635–648Google Scholar
  56. Hope PJ, Pyle D, Daniels CB, Chapman I, Horowitz M, Morley JE, Trayhurn P, Kumaratilake J, Wittert G (1997) Identification of brown fat and mechanisms for energy balance in the marsupial, Sminthopsis crassicaudata. Am J Physiol. 273(1 Pt 2):R161–7Google Scholar
  57. Horovitz I, Martin T, Bloch J, Ladevèze S, Kurz C, Sánchez-Villagra MR (2009) Cranial anatomy of the earliest marsupials and the origin of opossums. Plos One 4(12):e8278Google Scholar
  58. Hughes RL, Hall LS (1988) Structural adaptations of the newborn marsupial. In: Tyndale-Biscoe CH, PA Janssens (eds) The Developing Marsupial. Springer Verlag, Berlin, pp 8–27Google Scholar
  59. Isler K, CP van Schaik (2009) The expensive brain: a framework for explaining evolutionary changes in brain size. J Hum Evol 57:392–400PubMedCrossRefGoogle Scholar
  60. Jastroch M, Withers KW, Taudien S, Frappell PB, Helwig M, Fromme T, Hirschberg V, Heldmaier G, McAllan BM, Firth BT, Burmester T, Platzer M, Klingenspor M (2008) Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis. Physiol Genom 32:161–169CrossRefGoogle Scholar
  61. Jones ME (2003) Convergence in ecomorphology and guild structure among marsupial and placental carnivores. In: Jones ME, C Dickman, M Archer (eds) Predators with Pouches: The Biology of Carnivorous Marsupials. CSIRO Publishing, Collingwood, Victoria, pp 269–285Google Scholar
  62. Kay RF, MacFadden BJ, Madden RH, Sandeman H, Anaya F (1998) Revised age of the Salla beds, Bolivia, and its bearing on the age of the Deseadan South American Land Mammal ‘Age’. J Vertebr Paleontol 18:189–199CrossRefGoogle Scholar
  63. Kelly EM, Sears KE (2011a) Limb specialization in living marsupial and eutherian mammals: an investigation of constraints on mammalian limb evolution. J Mammal 92:1038–1049CrossRefGoogle Scholar
  64. Kelly EM, Sears KE (2011b) Reduced integration in marsupial limbs and the implications for mammalian evolution. Biol J Linn Soc 102:22–36CrossRefGoogle Scholar
  65. Keyte AL, Smith KK (2010) Developmental origins of precocial forelimbs in marsupial neonates. Development 137:4283–4294PubMedCrossRefGoogle Scholar
  66. Keyte AL, Smith KK (2012) Heterochrony in somitogenesis rate in a model marsupial, Monodelphis domestica. Evol Devel 14:93–103CrossRefGoogle Scholar
  67. Kirsch JAW (1977) The six-percent solution: second thoughts on the adaptedness of the Marsupialia. Am Sci 65:276–288PubMedGoogle Scholar
  68. Koenigswald WV, Goin FJ (2000) Enamel differentiation in South American marsupials and a comparison of placental and marsupial enamel. Paleontographica A255:129–168Google Scholar
  69. Koyabu D, Endo H, Mitgutsch C, Suwa G, Catania KC, Zollikofer CPE, Oda S, Koyasu K, Ando M, Sánchez-Villagra MR (2011) Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals. Evo Devo 2:21Google Scholar
  70. Lillegraven JA (1975) Biological considerations of the marsupial-placental dichotomy. Evolution 29:707–722CrossRefGoogle Scholar
  71. Lillegraven JA (2003) Polarities in mammalian evolution seen through homology of the inner cell mass. J Mammal Evol 10:277–333CrossRefGoogle Scholar
  72. Lillegraven JA, Thompson SD, McNab BK, Patton JL (1987) The origin of eutherian mammals. Biol J Linn Soc 32:281–336CrossRefGoogle Scholar
  73. Liow LH, Fortelius M, Lintulaakso K, Mannila H, Stenseth NC (2009) Lower extinction risk in sleep-or-hide mammals. Am Nat 178:264–272CrossRefGoogle Scholar
  74. Losos JB (2010) Adaptive radiation, ecological opportunity, and evolutionary determinism. Am Nat 175:623–639Google Scholar
  75. Luckett WP (1993) An ontogenetic assessment of dental homologies in therian mammals. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammalian Phylogeny: Mesozoic. Differentiation, Multituberculates, Monotremes, Early Therians and Marsupials. Springer, New York, pp 182–204Google Scholar
  76. Luo Z-X (2007) Transformation and diversification in the early mammalian evolution. Nature 450:1011–1019PubMedCrossRefGoogle Scholar
  77. Luo Z-X, Ji Q, Wible JR, Yuan C.-X (2003) An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302:1934–1940Google Scholar
  78. Luo Z-X, Yuan C-X, Meng Q-J, Ji Q (2011) A Jurassic eutherian mammal and the divergence of marsupials and placentals. Nature 476:442–445PubMedCrossRefGoogle Scholar
  79. Lynch VJ, Tanzer A, Wang Y, Leung FC, Gellersen B, Wagner GP (2008) Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc Natl Acad Sci USA 105:14928–14933PubMedCentralPubMedCrossRefGoogle Scholar
  80. Maridet O, Costeur L (2010) Diversity trends in Neogene European ungulates and rodents: large scale comparisons and perspectives. Naturwissenschaften 97:161–172PubMedCrossRefGoogle Scholar
  81. Marshall LG (2004) The terror birds of South America. Sci Am, Spec Ed 14: 82–89Google Scholar
  82. Martin GM, De Santis LJM, Moreira GJ (2008) Southernmost record for a living marsupial. Mammalia 72:131–134CrossRefGoogle Scholar
  83. McNab BK (2005) Uniformity in the basal metabolic rate of marsupials: its causes and consequences. Rev Chil Hist Nat 78:183–198Google Scholar
  84. McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol A 151:5–28CrossRefGoogle Scholar
  85. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simão TL, Stadler T, Rabosky DL, Honeycutt RL, Flynn JJ, Ingram CM, Steiner C, Williams TL, Robinson TJ, Burk-Herrick A, Westerman M, Ayoub NA, Springer MS, Murphy WJ (2011) Impacts of the Cretaceous terrestrial revolution and K/Pg extinction on mammal diversification. Science 334:521–524PubMedCrossRefGoogle Scholar
  86. Meredith RW, Westerman M, Case JA, Springer MS (2008) A phylogeny and timescale for marsupial evolution based on sequences for five nuclear genes. J Mammal Evol 15:1–36CrossRefGoogle Scholar
  87. Meslin C, Mugnier S, Callebaut I, Laurin M, Pascal G, Poupon A, Goudet G, Monget P (2012) Evolution of genes involved in gamete interaction: evidence for positive selection, duplications and losses in vertebrates. PLoS One 7(9): e44548.PubMedCentralPubMedCrossRefGoogle Scholar
  88. Mitgutsch C, Olsson L, Haas A (2009) Early embryogenesis in discoglossoid frogs: a study of heterochrony at different taxonomic levels. J Zool Syst Evol Res 47:248–257CrossRefGoogle Scholar
  89. Mitgutsch C, Richardson MK, Jiménez R, Martín JE, Kondrashov P, de Bakker MAG, Sánchez-Villagra MR (2012) Circumventing the pentadactyly ‘constraint’ - autopodial recruitment of pre-axial structures in true moles. Biol Lett 8:74–77Google Scholar
  90. Moczek AP, Sultan S, Foster S, Ledon-Rettig C, Dworkin I, Nijhout HF, Abouheif E, Pfennig D (2011) The role of developmental plasticity in evolutionary innovation. Proc Roy Soc B 278:2705–2713CrossRefGoogle Scholar
  91. Muizon C de (1991) La fauna de mamíferos de Tiupampa (Paleoceno Inferior, Formación Santa Lucía) Bolivia. In: Suarez-Soruco R (ed) Fósiles y Facies de Bolivia, Volúmen I Vertebrados, Revista Técnica de Yacimientos Petrolíferos Fiscales de Bolivia 12:575–624Google Scholar
  92. Muizon C de, Céspedes R (2012) The beginning of the age of therian mammals in South America: Tiupampa, a transition between Northern and Southern worlds in the basal Paleocene. In: Rosenberger AL, MF Tejedor (eds) Origins and Evolution of Cenozoic South American Mammals. Springer Verlag, BerlinGoogle Scholar
  93. 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
  94. Novacek MJ (1992) Mammal phylogeny: shaking the tree. Nature 356:121–125Google Scholar
  95. Oliveira EV, Goin FJ (2006) Marsupials do inicio do Terciário da Bacia de Itaboraí: origen, irradiação, e história biogeográfica. In: Caceres NC, Monteiro Filho ELA (eds) Marsupiais do Brasil. Biologia, Ecologia e Evoluçao, Ed. UFMS, Campo Grande, pp 299–320Google Scholar
  96. Parent CE, Crespi BJ (2006) Sequential colonization and rapid diversification of Galápagos’ endemic land snail genus Bulimulus (Gastropoda, Stylommatophora). Evolution 60:2311–2328PubMedGoogle Scholar
  97. Pascual R, Archer M, Ortiz Jaureguizar E, Prado JL, Godthelp H, Hand SJ (1992) First discovery of monotremes in South America. Nature 356:704–706CrossRefGoogle Scholar
  98. Patterson B, Pascual R (1972) The fossil mammal fauna of South America. In: Keast AN, Erk FC, Glass B (eds) Evolution, Mammals and Southern Continents. State University of New York Press, New York, pp 274–309Google Scholar
  99. Phillips MJ, Bennett TH, Lee MSY (2009) Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas. Proc Natl Acad Sci USA 106: 17089–17094PubMedCentralPubMedCrossRefGoogle Scholar
  100. Pigot AL, Phillimore AB, Owens IPF, Orme CDL (2010) The shape and temporal dynamics of phylogenetic trees arising from geographic speciation. Syst Biol 59:660–673PubMedCrossRefGoogle Scholar
  101. Pough FH, Janis CM, Heiser JB (2008) Vertebrate Life. 8th edition. Benjamin Cummings, New JerseyGoogle Scholar
  102. Prevosti FJ, Forasiepi AM, Zimicz NA (2011) The evolution of the Cenozoic terrestrial mammalian predator guild in South America: competition or replacement? J Mammal Evol. doi:10.1007/s:10914-011-9175-9
  103. Prevosti FJ, Turazzini GF, Ercoli MD, Hingst-Zaher E (2012) Mandible shape in marsupial and placental carnivorous mammals: a morphological comparative study using geometric morphometrics. Zool J Linn Soc 164:836–855CrossRefGoogle Scholar
  104. Rabosky DL, Alfaro ME (2010) Evolutionary bangs and whimpers: methodological advances and conceptual frameworks for studying exceptional diversification. Syst Biol 59:615–618PubMedCrossRefGoogle Scholar
  105. Renfree MB (1993) Ontogeny, genetic control, and phylogeny of female reproduction in monotreme and therian mammals. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials. Springer-Verlag, New York, pp 4–20CrossRefGoogle Scholar
  106. Richardson MK (1999) Vertebrate evolution: the developmental origins of adult variation. BioEssays 21:604–613PubMedCrossRefGoogle Scholar
  107. Richardson MK, Gobes S, Leeuwen A van, Poelman A, Pieau C, Sánchez-Villagra MR (2009) Heterochrony in limb evolution: developmental mechanisms and natural selection. J Exp Zool B Mol Dev Evol 312B:639–664Google Scholar
  108. Rose KD (2006) The Beginning of the Age of Mammals. Johns Hopkins University Press, BaltimoreGoogle Scholar
  109. Rougier GW, Apesteguía S, Gaetano L (2011) Highly specialized mammalian skulls from the Late Cretaceous of South America. Nature 479:98–102PubMedCrossRefGoogle Scholar
  110. Rougier GW, Wible JR, Novacek MJ (1998) New specimens of Deltatheridium, implications for the early history of marsupials. Nature 396:459–463PubMedCrossRefGoogle Scholar
  111. Rougier GW, Wible JR, Beck RMD, Apesteguía S (2012) The Miocene mammal Necrolestes demonstrates the survival of a Mesozoic non-therian lineage into the late Cenozoic of South America. Proc Natl Acad Sci USA 109:20053–20058PubMedCentralPubMedCrossRefGoogle Scholar
  112. Sánchez-Villagra MR, Goswami A, Weisbecker V, Mock O, Kuratani S (2008) Conserved relative timing of cranial ossification patterns in early mammalian evolution. Evol Devel 10:519–530CrossRefGoogle Scholar
  113. Sánchez-Villagra MR, Narita Y, Kuratani (2007) Thoracolumbar vertebral number: the first skeletal synapomorphy for afrotherian mammals. Syst Biodiv 5:1–7CrossRefGoogle Scholar
  114. Schulte P, Alegret L, Arenillas I, Arz JA, Barton PJ, Bown PR, Bralower TJ, Christeson GL, Claeys P, Cockell CS, Collins GS, Deutsch A, Goldin TJ, Goto K, Grajales-Nishimura JM, Grieve RA, Gulick SP, Johnson KR, Kiessling W, Koeberl C, Kring DA, MacLeod KG, Matsui T, Melosh J, Montanari A, Morgan JV, Neal CR, Nichols DJ, Norris RD, Pierazzo E, Ravizza G, Rebolledo-Vieyra M, Reimold WU, Robin E, Salge T, Speijer RP, Sweet AR, Urrutia-Fucugauchi J, Vajda V, Whalen MT, Willumsen PS (2010) The Chicxulub asteroid impact and mass extinction at the Cretaceous-Paleogene boundary. Science 27:1214–1218CrossRefGoogle Scholar
  115. Sears KE (2004) Constraints on the morphological evolution of marsupial shoulder girdles. Evolution 58:2353–2370PubMedGoogle Scholar
  116. Sears KE (2009) Differences in the timing of prechrondrogenic limb development in mammals: the marsupial-placental dichotomy resolved. Evolution 63:2193–2200PubMedCrossRefGoogle Scholar
  117. Sears KE, Behringer RR, Rasweiler JJ, Niswander LA (2006) The development of bat flight: morphologic and molecular evolution of bat forelimb digit. Proc Natl Acad Sci USA 103:6581–6586PubMedCentralPubMedCrossRefGoogle Scholar
  118. Simpson GG (1980) Splendid Isolation. The Curious History of South American Mammals. Yale University Press, New HavenGoogle Scholar
  119. Smith KK (2001a) Heterochrony revisited: the evolution of developmental sequences. Biol J Linn Soc 73:169–186CrossRefGoogle Scholar
  120. Smith KK (2001b) Early development of the neural plate, neural crest and facial region of marsupials. J Anat 199:121–131PubMedCentralPubMedCrossRefGoogle Scholar
  121. Springer MS, Stanhope MJ, Madsen O, de Jong WW (2004) Molecules consolidate the placental mammal tree. Trends Ecol Evol 19:430–438PubMedCrossRefGoogle Scholar
  122. Sumiyama K, Miyake T, Grimwood J, Stuart A, Dickson M, Schmutz J Ruddle F, Myers R, Amemiya CT (2012) Theria-specific homeodomain and cis-regulatory element evolution of the Dlx3–4 bigene cluster in 12 different mammalian species. J Exp Zool B Mol Dev Evol 318:639–50PubMedCentralPubMedCrossRefGoogle Scholar
  123. Tejedor MF, Goin FJ, Gelfo JN, López G, Bond M, Carlini AA, Scillato-Yané GJ, Woodburne MO, Chornogubsky L, Aragón E, Reguero MA, Czaplewski NJ, Vincon S, Martin GM, Ciancio MR (2009) New early Eocene mammalian fauna from western Patagonia, Argentina. Am Mus Novitates 3638:1–42CrossRefGoogle Scholar
  124. Tyndale-Biscoe H (2005) Life of Marsupials. CSIRO Publishing, CollingwoodGoogle Scholar
  125. Ungar PS (2010) Mammal Teeth. John Hopkins University Press, BaltimoreGoogle Scholar
  126. Vaglia JL, Smith KK (2003) Early differentiation and migration of cranial neural crest in the opossum, Monodelphis domestica. Evol Devel 5:121–135CrossRefGoogle Scholar
  127. van Nievelt AFH, Smith KK (2005) To replace or not to replace: the significance of reduced tooth replacement in marsupial and placental mammals. Paleobiology 31:324–346CrossRefGoogle Scholar
  128. Voss RS, Jansa SA (2009) Phylogenetic relationships and classification of didelphid marsupials, an extant radiation of New World metatherian mammals. Bull Am Mus Natl Hist 322:1–177CrossRefGoogle Scholar
  129. Vullo R, Gheerbrant E, Muizon C de, Néraudeau D (2009) The oldest modern therian mammal from Europe and its bearing on stem marsupial paleobiogeography. Proc Natl Acad Sci USA 106:19910–19915Google Scholar
  130. Wagner A (2011) The Origins of Evolutionary Innovations. Oxford University Press, OxfordCrossRefGoogle Scholar
  131. Weisbecker V (2011) Monotreme ossification sequences and the riddle of mammalian skeletal development. Evolution 65: 1323–1335PubMedCrossRefGoogle Scholar
  132. Weisbecker V, Goswami A (2010) Brain size, life history, and metabolism at the marsupial/placental dichotomy. Proc Natl Acad Sci USA 107:16216–16221PubMedCentralPubMedCrossRefGoogle Scholar
  133. Weisbecker V, Goswami A, Wroe S, Sánchez-Villagra MR (2008) Ossification heterochrony in the mammalian postcranial skeleton and the marsupial-placental dichotomy. Evolution 62:2027–2041PubMedCrossRefGoogle Scholar
  134. Werdelin L (1987) Jaw geometry and molar morphology in marsupial carnivores: analysis of a constraint and its macroevolutionary consequences. Paleobiology 13:342–350Google Scholar
  135. Werdelin L (1988) Circumventing a constraint - the case of Thylacoleo (Marsupialia, Thylacoleonidae). Austral J Zool 36:565–571CrossRefGoogle Scholar
  136. Wiens JJ (2011) The causes of species richness patterns across space, time, and clades and the role of “ecological limits”. Quart Rev Biol 86:75–96Google Scholar
  137. Wilson GP (2005) Mammalian faunal dynamics during the last 1.8 million years of the Cretaceous in Garfield County, Montana. J Mammal Evol 12:53–76CrossRefGoogle Scholar
  138. Wilson DE, Reeder DM (2005) Mammal Species of the World. Third Edition. Johns Hopkins University Press, BaltimoreGoogle Scholar
  139. Wilson GP, Dechesne M, Anderson I (2010) New latest Cretaceous mammals from northeastern Colorado with biochronologic and biogeographic implications. J Vertebr Paleontol 30:499–520.CrossRefGoogle Scholar
  140. Wilson GP, Evans AR, Corfe IJ, Smits PD, Fortelius M, Jernvall J (2012) Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature 483:457–460PubMedCrossRefGoogle Scholar
  141. Wilson LAB, Sánchez-Villagra MR (2010) Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents. Proc Roy Soc B 277:1227–1234CrossRefGoogle Scholar
  142. Woodburne M (2010) The Great American Biotic Interchange: dispersals, tectonics, climate, sea level, and holding pens. J Mammal Evol 17:245–264PubMedCentralPubMedCrossRefGoogle Scholar
  143. 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
  144. Woodburne MO, Zinsmeister WJ (1982) Fossil land mammal from Antarctica. Science 218:284–285PubMedCrossRefGoogle Scholar
  145. Wroe S, Archer M (1995) Extraordinary diphyodonty-related change in dental function for a tooth of the extinct marsupial Ekaltadeta ima (Propleopinae, Hypsiprymnodontidae). Arch Oral Biol 40:597–603PubMedCrossRefGoogle Scholar
  146. Wroe S, Argot C, Dickman C (2004a) On the rarity of big fierce carnivores and primacy of isolation and area: tracking large mammalian carnivore diversity on two isolated continents. Proc Roy Soc B 271:1203–1211CrossRefGoogle Scholar
  147. Wroe S, Brammall J, Cooke BN (1998) The skull of Ekaltadeta ima (Marsupialia: Hypsiprymnodontidae?): an analysis of some cranial features among marsupials and a re-investigation of propleopine phylogeny, with notes on the inference of carnivory in mammals. J Paleontol 72:738–751CrossRefGoogle Scholar
  148. Wroe S, Crowther M, Dortch J, Chong J (2004b) The size of the largest marsupial and why it matters. Proc Roy Soc B (Suppl) 271:34–S36CrossRefGoogle Scholar
  149. Wroe S, Milne N (2007) Convergence and remarkably consistent constraint in the evolution of carnivore skull shape. Evolution 61:1251–1260PubMedCrossRefGoogle Scholar
  150. Wroe S, Myers T, Seebacher F, Kear B, Gillespie A, Crowther M, Salisbury S (2003) An alternative method for predicting body-mass: the case of the marsupial lion, Thylacoleo carnifex. Paleobiology 29:404–412CrossRefGoogle Scholar
  151. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693Google Scholar
  152. Zack S, Penkrot TA, Bloch JI, Rose KD (2005) Affinities of ‘hyopsodontids’ to elephant shrews and a Holarctic origin of Afrotheria. Nature 434:497–501Google Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  1. 1.Paläontologisches Institut und MuseumUniversität ZürichZürichSwitzerland

Personalised recommendations