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Transformation and diversification in early mammal evolution

Abstract

Evolution of the earliest mammals shows successive episodes of diversification. Lineage-splitting in Mesozoic mammals is coupled with many independent evolutionary experiments and ecological specializations. Classic scenarios of mammalian morphological evolution tend to posit an orderly acquisition of key evolutionary innovations leading to adaptive diversification, but newly discovered fossils show that evolution of such key characters as the middle ear and the tribosphenic teeth is far more labile among Mesozoic mammals. Successive diversifications of Mesozoic mammal groups multiplied the opportunities for many dead-end lineages to iteratively evolve developmental homoplasies and convergent ecological specializations, parallel to those in modern mammal groups.

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Figure 1: Phylogeny and diversification of Mesozoic and major extant mammal groups.
Figure 2: Diverse evolutionary experiments of Mesozoic mammals and their ecological convergence to modern mammal ecomorphotypes.
Figure 3: Evolution of the mammalian cranio-mandibular joint and the definitive mammalian middle ear through the cynodont–mammal transition.
Figure 4: Convergent and iterative evolution of protocones and pseudo-protocones in Mesozoic mammals.

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References

  1. Kielan-Jaworowska, Z. et al. Mammals from the Age of Dinosaurs—Origins, Evolution, and Structure (Columbia Univ. Press, New York, 2004)

    Google Scholar 

  2. Kemp, T. S. The Origin And Evolution of Mammals (Oxford Univ. Press, Oxford, 2005)

    Google Scholar 

  3. Lillegraven, J. A., Kielan-Jaworowska, Z. & Clemens, W. A. (eds) Mesozoic Mammals: The First Two-thirds of Mammalian History (Univ. Calif. Press, Berkeley, 1979)

    Google Scholar 

  4. McKenna, M. C. & Bell, S. K. Classification of Mammals Above the Species Level (Columbia Univ. Press, New York, 1997)

    Google Scholar 

  5. Wang, C. S. & Dodson, P. Estimating the diversity of dinosaurs. Proc. Natl Acad. Sci. USA 103, 13601–13605 (2006)

    CAS  PubMed  ADS  Google Scholar 

  6. Hopson, J. A. & Kitching, J. W. A probainognathian cynodont from South Africa and the phylogeny of nonmammalian cynodonts. Bull. Mus. Comp. Zool. (Harvard) 156, 5–35 (2001)

    Google Scholar 

  7. Rowe, T. B. Definition, diagnosis, and origin of Mammalia. J. Vertebr. Paleontol. 8, 241–264 (1988)

    Google Scholar 

  8. Sidor, C. A. Simplification as a trend in synapsid cranial evolution. Evolution Int. J. Org. Evolution 55, 1419–1442 (2001)

    CAS  Google Scholar 

  9. Sidor, C. A. & Hopson, J. A. Ghost lineages and “mammalness”: assessing the temporal pattern of character acquisition in the Synapsida. Paleobiology 24, 254–273 (1998)

    Google Scholar 

  10. Rougier, G. W. et al. Implications of Deltatheridium specimens for early marsupial history. Nature 396, 459–463 (1998)

    CAS  PubMed  ADS  Google Scholar 

  11. Luo, Z.-X. et al. An Early Cretaceous tribosphenic mammal and metatherian evolution. Science 302, 1934–1940 (2003)

    CAS  PubMed  ADS  Google Scholar 

  12. Asher, R. J. et al. First combined cladistic analysis of marsupial mammal interrelationships. Mol. Phylogenet. Evol. 33, 240–250 (2004)

    CAS  PubMed  Google Scholar 

  13. Asher, R. J. et al. Stem Lagomorpha and the antiquity of Glires. Science 307, 1091–1094 (2005)

    CAS  PubMed  ADS  Google Scholar 

  14. Wible, J. R. et al. Cretaceous eutherians and Laurasian origin for placental mammals near the K-T boundary. Nature 442, 1003–1006 (2007)

    ADS  Google Scholar 

  15. Archibald, J. D. et al. Late Cretaceous relatives of rabbits, rodents, and other extant eutherian mammals. Nature 414, 62–65 (2001)

    CAS  PubMed  ADS  Google Scholar 

  16. Simpson, G. G. A Catalogue of the Mesozoic Mammalia in the Geological Department of the British Museum (British Museum, London, 1928)

    Google Scholar 

  17. Kemp, T. S. The relationships of mammals. Zool. J. Linn. Soc. 77, 353–384 (1983)

    Google Scholar 

  18. Wible, J. R. & Hopson, J. A. in Mammal Phylogeny Vol. 1 (eds F. S. Szalay et al.) 45–62 (Springer-Verlag, New York, 1993)

    Google Scholar 

  19. Luo, Z.-X. et al. In quest for a phylogeny of Mesozoic mammals. Acta Palaeontol. Polonica 47, 1–78 (2002)

    Google Scholar 

  20. Luo, Z.-X. & Wible, J. R. A new Late Jurassic digging mammal and early mammalian diversification. Science 308, 103–107 (2005)

    CAS  PubMed  ADS  Google Scholar 

  21. Luo, Z.-X. et al. A new eutriconodont mammal and evolutionary development of early mammals. Nature 446, 288–293 (2007)

    CAS  PubMed  ADS  Google Scholar 

  22. Cifelli, R. L. Early mammalian radiations. J. Paleontol. 75, 1214–1226 (2001)

    Google Scholar 

  23. Murphy, W. J. et al. Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294, 2348–2351 (2001)

    CAS  PubMed  ADS  Google Scholar 

  24. Springer, M. S. et al. Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc. Natl Acad. Sci. USA 100, 1056–1061 (2003)

    CAS  PubMed  ADS  Google Scholar 

  25. Nilsson, M. A. et al. Marsupial relationships and a timeline for marsupial radiation in South Gondwana. Gene 340, 189–196 (2004)

    CAS  PubMed  Google Scholar 

  26. Bininda-Emonds, O. R. P. et al. The delayed rise of present-day mammals. Nature 446, 507–512 (2007)

    CAS  PubMed  ADS  Google Scholar 

  27. Benton, M. J. & Donoghue, P. C. J. Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26–53 (2007)

    CAS  PubMed  Google Scholar 

  28. Archibald, J. D. & Deutschman, D. H. Quantitative analysis of the timing of the origin and diversification of extant placental orders. J. Mamm. Evol. 8, 107–124 (2001)

    Google Scholar 

  29. Foote, M. et al. Evolutionary and preservational constraints on origins of biologic groups: divergence times of eutherian mammals. Science 283, 1310–1314 (1999)

    CAS  PubMed  ADS  Google Scholar 

  30. Hunter, J. P. & Janis, C. M. Spiny Norman in the Garden of Eden? Dispersal and early biogeography of Placentalia. J. Mamm. Evol. 13, 89–123 (2006)

    Google Scholar 

  31. Easteal, S. Molecular evidence for the early divergence of placental mammals. BioEssays 21, 1052–1058 (1999)

    CAS  PubMed  Google Scholar 

  32. Bromham, L. et al. Growing up with dinosaurs: molecular dates and the mammalian radiation. Trends Ecol. Evol. 14, 113–118 (1999)

    CAS  PubMed  Google Scholar 

  33. Wesley-Hunt, G. D. The morphological diversification of carnivores in North America. Paleobiology 31, 35–55 (2005)

    Google Scholar 

  34. Zhou, Z.-H. et al. An exceptionally preserved Lower Cretaceous ecosystem. Nature 421, 807–814 (2003)

    CAS  PubMed  ADS  Google Scholar 

  35. Jenkins, F. A. & Parrington, F. R. The postcranial skeletons of the Triassic mammals Eozostrodon, Megazostrodon and Erythrotherium . Phil. Trans. R. Soc. Lond. B 273, 387–431 (1976)

    ADS  Google Scholar 

  36. Damiani, R. et al. Earliest evidence of cynodont burrowing. Proc. R. Soc. Lond. B 270, 1747–1751 (2003)

    Google Scholar 

  37. Kielan-Jaworowska, Z. & Gambaryan, P. P. Postcranial anatomy and habits of Asian multituberculate mammals. Fossils Strata 36, 1–92 (1994)

    Google Scholar 

  38. Ji, Q. et al. A swimming mammaliaform from the Middle Jurassic and ecomorphological diversification of early mammals. Science 311, 1123–1127 (2006)

    CAS  PubMed  ADS  Google Scholar 

  39. Martin, T. Postcranial anatomy of Haldanodon exspectatus (Mammalia, Docodonta) from the Late Jurasssic (Kimmeridgian) of Portugal and its bearing for mammalian evolution. Zool. J. Linn. Soc. 145, 219–248 (2005)

    Google Scholar 

  40. Martin, T. Paleontology: early mammalian evolutionary experiments. Science 311, 1109–1110 (2006)

    CAS  PubMed  Google Scholar 

  41. Luo, Z.-X. et al. A new mammaliaform from the Early Jurassic of China and evolution of mammalian characteristics. Science 292, 1535–1540 (2001)

    CAS  PubMed  ADS  Google Scholar 

  42. Hu, Y.-M. et al. Large Mesozoic mammals fed on young dinosaurs. Nature 433, 149–153 (2005)

    CAS  PubMed  ADS  Google Scholar 

  43. Szalay, F. S. & Sargis, E. J. Model-based analysis of postcranial osteology of marsupials from the Palaeocene of Itaboraí (Brazil) and the phylogenetics and biogeography of Metatheria. Geodiversitas 23, 139–302 (2001)

    Google Scholar 

  44. Muizon, C. de. Mayulestes ferox, a borhyaenoid (Metatheria, Mammalia) from the early Palaeocene of Bolivia. Phylogenetic and palaeobiologic implications. Geodiversitas 20, 19–142 (1998)

    Google Scholar 

  45. Argot, C. Functional–adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus . J. Morphol. 247, 51–79 (2001)

    CAS  PubMed  Google Scholar 

  46. Krause, D. W. & Jenkins, F. A. The postcranial skeleton of North American multituberculates. Bull. Mus. Comp. Zool. Harv. 150, 199–246 (1983)

    Google Scholar 

  47. Krebs, B. Das Skelett von Henkelotherium guimarotae gen. et sp. nov. (Eupantotheria, Mammalia) aus dem Oberen Jura von Portugal. Berliner Geowissensch. Abh. A133, 1–110 (1991)

    Google Scholar 

  48. Ji, Q. et al. The earliest-known eutherian mammal. Nature 416, 816–822 (2002)

    CAS  PubMed  ADS  Google Scholar 

  49. Meng, J. et al. A Mesozoic gliding mammal from northeastern China. Nature 444, 889–893 (2006)

    CAS  PubMed  ADS  Google Scholar 

  50. Luo, Z.-X. in In the Shadow of the Dinosaurs—Early Mesozoic Tetrapods (eds N. C. Fraser & H.-D. Sues) 98–128 (Cambridge Univ. Press, Cambridge, 1994)

    Google Scholar 

  51. Luo, Z.-X. & Crompton, A. W. Transformation of the quadrate (incus) through the transition from non-mammalian cynodonts to mammals. J. Vertebr. Paleontol. 14, 341–374 (1994)

    Google Scholar 

  52. Crompton, A. W. in Studies in Vertebrate Evolution (eds K. A. Joysey & T. S. Kemp) 231–253 (Oliver & Boyd, Edinburgh, 1972)

    Google Scholar 

  53. Kermack, K. A. et al. The lower jaw of Morganucodon . Zool. J. Linn. Soc. 53, 87–175 (1973)

    Google Scholar 

  54. Kermack, K. A. et al. The skull of Morganucodon . Zool. J. Linn. Soc. 71, 1–158 (1981)

    Google Scholar 

  55. Allin, E. F. & Hopson, J. A. in The Evolutionary Biology of Hearing (eds Webster, D. B. et al.) 587–614 (Springer, New York, 1992)

    Google Scholar 

  56. Rowe, T. B. Coevolution of the mammalian middle ear and neocortex. Science 273, 651–654 (1996)

    CAS  PubMed  ADS  Google Scholar 

  57. Bonaparte, J. F. et al. New information on Brasilodon and Brasilitherium (Cynodontia, Probainognathia) from the Late Triassic, southern Brazil. Revist. Brasil. Paleontol. 8, 25–56 (2005)

    Google Scholar 

  58. Gaupp, E. Die Reichertsche Theorie (Hammer-, Amboss- und Kieferfrage). Archiv. Anatomie Entwick. 1912, 1–426 (1913)

    Google Scholar 

  59. Zeller, U. Die Entwicklung und Morphologie des Schädels von Ornithorhynchus anatinus (Mammalia: Prototheria: Monotremata). Abh. Senckenberg. Naturforsch. Ges. 545, 1–188 (1989)

    Google Scholar 

  60. Maier, W. Phylogeny and ontogeny of mammalian middle ear structures. Nether. J. Zool. 40, 55–75 (1990)

    Google Scholar 

  61. Maier, W. in Mammal Phylogeny Vol. 1 (eds Szalay, F. S. et al.) 165–181 (Springer, New York, 1993)

    Google Scholar 

  62. Sánchez-Villagra, M. R. et al. Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals. J. Morphol. 251, 219–238 (2002)

    PubMed  Google Scholar 

  63. Bever, G. et al. Comment on “Independent origins of middle ear bones in monotremes and therians.”. Science 309, 1492a (2005)

    Google Scholar 

  64. Rougier G. W, Forasiepi, A. M. & Martinelli, A. G. Comment on “Independent origins of middle ear bones in monotremes and therians.”. Science 309, 1492b (2005)

    Google Scholar 

  65. Rich, T. H. et al. Independent origins of middle ear bones in monotremes and therians. Science 307, 910–914 (2005)

    CAS  PubMed  ADS  Google Scholar 

  66. Martin, T. & Luo, Z.-X. Paleontology: homoplasy in the mammalian ear. Science 307, 861–862 (2005)

    CAS  PubMed  Google Scholar 

  67. Wang, Y.-Q. et al. An ossified Meckel’s cartilage in two Cretaceous mammals and origin of the mammalian middle ear. Science 294, 357–361 (2001)

    CAS  PubMed  ADS  Google Scholar 

  68. Li, C.-K. et al. A new species of Gobiconodon (Triconodonta, Mammalia) and its implication for the age of Jehol Biota. Chin. Sci. Bull. [English]. 48, 1129–1134 (2003)

    Google Scholar 

  69. Meng, J. et al. The ossified Meckel’s cartilage and internal groove in Mesozoic mammaliaforms: implications to origin of the definitive mammalian middle ear. Zool. J. Linn. Soc. 138, 431–448 (2003)

    Google Scholar 

  70. Patterson, B. Early Cretaceous mammals and the evolution of mammalian molar teeth. Fieldiana. Geology 13, 1–105 (1956)

    Google Scholar 

  71. Crompton, A. W. in Early Mammals (eds Kermack, D. M. & Kermack, K. A.) 65–87 (Zool. J. Linn. Soc., London, 1971)

    Google Scholar 

  72. McKenna, M. C. in Phylogeny of the Primates (eds Luckett, W. P. & Szalay, F. S.) 21–46 (Plenum Publ. Corp., New York, 1975)

    Google Scholar 

  73. Prothero, D. R. New Jurassic mammals from Como Bluff, Wyoming, and the interrelationships of non-tribosphenic Theria. Bull. Am. Mus. Nat. Hist. 167, 277–326 (1981)

    Google Scholar 

  74. Lopatin, A. V. & Averianov, A. O. An aegialodontid upper molar and the evolution of mammal dentition. Science 313, 1092 (2006)

    CAS  PubMed  Google Scholar 

  75. Chow, M. & Rich, T. H. Shuotherium dongi, n. gen. and sp., a therian with pseudo-tribosphenic molars from the Jurassic of Sichuan, China. Austral. Mamm. 5, 127–142 (1982)

    Google Scholar 

  76. Sigogneau-Russell, D. Discovery of a Late Jurassic Chinese mammal in the upper Bathonian of England. C. R. Acad. Sci. II 327, 571–576 (1998)

    Google Scholar 

  77. Wang, Y.-Q. et al. A probable pseudo-tribosphenic upper molar from the Late Jurassic of China and the early radiation of the Holotheria. J. Vertebr. Paleontol. 18, 777–787 (1998)

    Google Scholar 

  78. Luo, Z. X. et al. Convergent dental evolution in pseudotribosphenic and tribosphenic mammals. Nature 450, 93–97 (2007)

    CAS  PubMed  ADS  Google Scholar 

  79. Rich, T. H. et al. A tribosphenic mammal from the Mesozoic of Australia. Science 278, 1438–1442 (1997)

    CAS  PubMed  ADS  Google Scholar 

  80. Rich, T. H. et al. An advanced ausktribosphenid from the Early Cretaceous of Australia. Rec. Queen Victoria Mus. 110, 1–9 (2001)

    Google Scholar 

  81. Flynn, J. J. et al. A Middle Jurassic mammal from Madagascar. Nature 401, 57–60 (1999)

    CAS  ADS  Google Scholar 

  82. Rauhut, O. W. M. et al. A Jurassic mammal from South America. Nature 416, 165–168 (2002)

    CAS  PubMed  ADS  Google Scholar 

  83. Martin, T. & Rauhut, O. W. M. Mandible and dentition of Asfaltomylos patagonicus (Australosphenida, Mammalia) and the evolution of tribosphenic teeth. J. Vertebr. Paleontol. 25, 414–425 (2005)

    Google Scholar 

  84. Rougier, G. W. et al. New Jurassic mammals from Patagonia, Argentina: a reappraisal of australosphenidan morphology and interrelationship. Am. Mus. Novitates 3566, 1–54 (2007)

    Google Scholar 

  85. Luo, Z.-X. et al. Dual origin of tribosphenic mammals. Nature 409, 53–57 (2001)

    CAS  PubMed  ADS  Google Scholar 

  86. Rich, T. H. et al. Evidence that monotremes and ausktribosphenids are not sistergroups. J. Vertebr. Paleontol. 22, 466–469 (2002)

    Google Scholar 

  87. Woodburne, M. O. Monotremes as pretribosphenic mammals. J. Mamm. Evol. 10, 195–248 (2003)

    Google Scholar 

  88. Musser, A. M. Investigations into the Evolution of Australian Mammals with a Focus on Monotremata PhD thesis, Univ. of New South Wales. (2006)

    Google Scholar 

  89. Sigogneau-Russell, D. et al. The oldest tribosphenic mammal from Laurasia (Purbeck Limestone Group, Berriasian, Cretaceous, UK) and its bearing on the “dual origin” of Tribosphenida. Comptes. Rend. Acad. Sci. 333, 141–147 (2001)

    Google Scholar 

  90. Sigogneau-Russell, D. Docodonts from the British Mesozoic. Acta Palaeontol. Polonica 48, 357–374 (2003)

    Google Scholar 

  91. Evans, A. R. & Sanson, G. D. The tooth of perfection: functional and spatial constraints on mammalian tooth shape. Biol. J. Linn. Soc. 78, 173–191 (2003)

    Google Scholar 

  92. Kangas, A. T. et al. Nonindependence of mammalian dental characters. Nature 432, 211–214 (2004)

    CAS  PubMed  ADS  Google Scholar 

  93. Kassai, Y. et al. Regulation of mammalian tooth cusp patterning by ectodin. Science 309, 2067–2070 (2005)

    CAS  PubMed  ADS  Google Scholar 

  94. Jenkins, F. A. The postcranial skeleton of African cynodonts. Peabody Mus. Nat. Hist. Bull. 36, 1–216 (1971)

    Google Scholar 

  95. Filler, A. G. Axial Character Seriation in Mammals: an Historical and Morphological Exploration of the Origin, Development, Use and Current Collapse of the Homology Paradigm PhD thesis, Harvard Univ. (1986)

    Google Scholar 

  96. Narita, Y. & Kuratani, S. Evolution of vertebral formulae in mammals: a perspective on developmental constraints. J. Exp. Zool. 304B, 91–106 (2005)

    Google Scholar 

  97. Wellik, D. M. & Capecchi, M. R. Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 301, 363–367 (2003)

    CAS  PubMed  ADS  Google Scholar 

  98. Li, G. & Luo, Z.-X. A Cretaceous symmetrodont therian with some monotreme-like postcranial features. Nature 439, 195–200 (2006)

    CAS  PubMed  ADS  Google Scholar 

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Acknowledgements

I benefited from years of stimulating discussion about early mammal evolution with R. Cifelli, T. Martin, J. Wible, Z. Kielan-Jaworowska, T. Rowe, H. Sues, M. Dawson, K. C. Beard, G. Wilson, G. Rougier, J. Bonaparte, W. Maier, P.-J. Chen and Q. Ji, and discussion on diversification pattern with D. Erwin and M. Benton. Many helped my research: A. Tabrum, X.-N. Yang, Q. Yang, P.-J. Chen, Z.-M. Dong, K.-Q. Gao. I thank Q. Ji and J. R. Wible for access to comparative collections; M. R. Dawson, T. Martin and J. R. Wible for improving the manuscript; M. Klingler for assistance with graphics. Support was from the National Science Foundation (USA), National Natural Science Foundation of China, National Geographic Society and the Carnegie Museum.

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Luo, ZX. Transformation and diversification in early mammal evolution. Nature 450, 1011–1019 (2007). https://doi.org/10.1038/nature06277

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