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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

References

  1. 1

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

  2. 2

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

  3. 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)

  4. 4

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

  5. 5

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

  6. 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)

  7. 7

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

  8. 8

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

  9. 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)

  10. 10

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

  11. 11

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

  12. 12

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

  13. 13

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

  14. 14

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

  15. 15

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

  16. 16

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

  17. 17

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

  18. 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)

  19. 19

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

  20. 20

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

  21. 21

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

  22. 22

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

  23. 23

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

  24. 24

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

  25. 25

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

  26. 26

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

  27. 27

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

  28. 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)

  29. 29

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

  30. 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)

  31. 31

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

  32. 32

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

  33. 33

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

  34. 34

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

  35. 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)

  36. 36

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

  37. 37

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

  38. 38

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

  39. 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)

  40. 40

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

  41. 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)

  42. 42

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

  43. 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)

  44. 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)

  45. 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)

  46. 46

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

  47. 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)

  48. 48

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

  49. 49

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

  50. 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)

  51. 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)

  52. 52

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

  53. 53

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

  54. 54

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

  55. 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)

  56. 56

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

  57. 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)

  58. 58

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

  59. 59

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

  60. 60

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

  61. 61

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

  62. 62

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

  63. 63

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

  64. 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)

  65. 65

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

  66. 66

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

  67. 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)

  68. 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)

  69. 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)

  70. 70

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

  71. 71

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

  72. 72

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

  73. 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)

  74. 74

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

  75. 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)

  76. 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)

  77. 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)

  78. 78

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

  79. 79

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

  80. 80

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

  81. 81

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

  82. 82

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

  83. 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)

  84. 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)

  85. 85

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

  86. 86

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

  87. 87

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

  88. 88

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

  89. 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)

  90. 90

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

  91. 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)

  92. 92

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

  93. 93

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

  94. 94

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

  95. 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)

  96. 96

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

  97. 97

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

  98. 98

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

Download references

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.

Author information

Correspondence to Zhe-Xi Luo.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.