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Adaptive radiation of multituberculate mammals before the extinction of dinosaurs

Abstract

The Cretaceous–Paleogene mass extinction approximately 66 million years ago is conventionally thought to have been a turning point in mammalian evolution1,2. Prior to that event and for the first two-thirds of their evolutionary history, mammals were mostly confined to roles as generalized, small-bodied, nocturnal insectivores3, presumably under selection pressures from dinosaurs4. Release from these pressures, by extinction of non-avian dinosaurs at the Cretaceous–Paleogene boundary, triggered ecological diversification of mammals1,2. Although recent individual fossil discoveries have shown that some mammalian lineages diversified ecologically during the Mesozoic era5, comprehensive ecological analyses of mammalian groups crossing the Cretaceous–Paleogene boundary are lacking. Such analyses are needed because diversification analyses of living taxa6,7 allow only indirect inferences of past ecosystems. Here we show that in arguably the most evolutionarily successful clade of Mesozoic mammals, the Multituberculata, an adaptive radiation began at least 20 million years before the extinction of non-avian dinosaurs and continued across the Cretaceous–Paleogene boundary. Disparity in dental complexity, which relates to the range of diets, rose sharply in step with generic richness and disparity in body size. Moreover, maximum dental complexity and body size demonstrate an adaptive shift towards increased herbivory. This dietary expansion tracked the ecological rise of angiosperms8 and suggests that the resources that were available to multituberculates were relatively unaffected by the Cretaceous–Paleogene mass extinction. Taken together, our results indicate that mammals were able to take advantage of new ecological opportunities in the Mesozoic and that at least some of these opportunities persisted through the Cretaceous–Paleogene mass extinction. Similar broad-scale ecomorphological inventories of other radiations may help to constrain the possible causes of mass extinctions9,10.

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Figure 1: Dental and dietary diversity in multituberculate mammals.
Figure 2: Temporal patterns of multituberculate dental complexity, taxonomic richness, body size and angiosperm ecological diversification.

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References

  1. Alroy, J. The fossil record of North American mammals: evidence for a Paleocene evolutionary radiation. Syst. Biol. 48, 107–118 (1999)

    Article  CAS  Google Scholar 

  2. Smith, F. A. et al. The evolution of maximum body size of terrestrial mammals. Science 330, 1216–1219 (2010)

    Article  ADS  CAS  Google Scholar 

  3. Kielan-Jaworowska, Z., Cifelli, R. L. & Luo, Z.-X. Mammals from the Age of Dinosaurs: Origins, Evolution, and Structure (Columbia Univ. Press, 2004)

    Book  Google Scholar 

  4. Van Valen, L. M. & Sloan, R. E. Ecology and the extinction of the dinosaurs. Evol. Theory 2, 37–64 (1977)

    Google Scholar 

  5. Luo, Z.-X. Transformation and diversification in early mammalian evolution. Nature 450, 1011–1019 (2007)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  7. Meredith, R. W. et al. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334, 521–524 (2011)

    Article  ADS  CAS  Google Scholar 

  8. Wing, S. L. & Boucher, L. D. Ecological aspects of the Cretaceous flowering plant radiation. Annu. Rev. Earth Planet. Sci. 26, 379–421 (1998)

    Article  ADS  CAS  Google Scholar 

  9. Archibald, J. D. et al. Cretaceous extinctions: multiple causes. Science 328, 973 (2010)

    Article  CAS  Google Scholar 

  10. Schulte, P. et al. The Chicxulub asteroid impact and mass extinction at the Cretaceous-Paleogene boundary. Science 327, 1214–1218 (2010)

    Article  ADS  CAS  Google Scholar 

  11. Weil, A. & Krause, D. W. in Evolution of Tertiary Mammals of North America Vol. 2 (eds Janis, C. M., Gunnell, G.F. & Uhen, M. D. ) 19–38 (Cambridge Univ. Press, 2008)

    Book  Google Scholar 

  12. Krause, D. W. in Vertebrates, Phylogeny, and Philosophy (eds Flanagan, K.M. & Lillegraven, J.A. ) 119–130 (Contributions to Geology, 1986)

    Google Scholar 

  13. Rich, T. H. et al. An Australian multituberculate and its palaeobiogeographic implications. Acta Palaeontol. Pol. 54, 1–6 (2009)

    Article  Google Scholar 

  14. Gingerich, P. D. in Patterns of Evolution (ed. Hallam, A. ) 469–500 (Elsevier, 1977)

    Google Scholar 

  15. Krause, D. W. Jaw movement, dental function, and diet in the Paleocene multituberculate Ptilodus. Paleobiology 8, 265–281 (1982)

    Article  Google Scholar 

  16. Cope, E. D. The tertiary Marsupialia. Am. Nat. 18, 686–697 (1884)

    Article  Google Scholar 

  17. Simpson, G. G. The “plagiaulacoid” type of mammalian dentition. J. Mamm. 14, 97–107 (1933)

    Article  Google Scholar 

  18. Evans, A. R., Wilson, G. P., Fortelius, M. & Jernvall, J. High-level similarity of dentitions in carnivorans and rodents. Nature 445, 78–81 (2007)

    Article  ADS  CAS  Google Scholar 

  19. Santana, S. E., Strait, S. & Dumont, E. R. The better to eat you with: functional correlates of tooth structure in bats. Funct. Ecol. 25, 839–847 (2011)

    Article  Google Scholar 

  20. Jernvall, J., Gilbert, C. C. & Wright, P. C. in Elwyn Simons: A Search for Origins (eds Fleagle, J. G. & Gilbert, C. C. ) 335–342 (Springer, 2008)

    Book  Google Scholar 

  21. Prideaux, G. J. Systematics and evolution of the sthenurine kangaroos. Univ. Calif. Publ. Geol. Sci. 146, 1–622 (2004)

    Google Scholar 

  22. Barrett, P. M., McGowan, A. J. & Page, V. Dinosaur diversity and the rock record. Proc. R. Soc. B 276, 2667–2674 (2009)

    Article  Google Scholar 

  23. Foote, M. The evolution of morphological diversity. Annu. Rev. Ecol. Syst. 28, 129–152 (1997)

    Article  Google Scholar 

  24. Lupia, R., Lidgard, S. & Crane, P. R. Comparing palynological abundance and diversity: implications for biotic replacement during the Cretaceous angiosperm radiation. Paleobiology 25, 305–340 (1999)

    Article  Google Scholar 

  25. Feild, T. S. et al. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proc. Natl Acad. Sci. USA 108, 8363–8366 (2011)

    Article  ADS  CAS  Google Scholar 

  26. Wing, S. L. & Tiffney, B. H. in The Origins of Angiosperms and Their Biological Consequences (eds Friis, E.M.,, Chaloner, W.G. & Crane, P.R. ) 203–224 (Cambridge Univ. Press, 1987)

    Google Scholar 

  27. Schneider, H. et al. Ferns diversified in the shadow of angiosperms. Nature 428, 553–557 (2004)

    Article  ADS  CAS  Google Scholar 

  28. Grimaldi, D. The co-radiations of pollinating insects and angiosperms in the Cretaceous. Ann. Mo. Bot. Gard. 86, 373–406 (1999)

    Article  Google Scholar 

  29. Wilson, G. P. Mammalian faunal dynamics during the last 1.8 million years of the Cretaceous in Garfield County, Montana. J. Mamm. Evol. 12, 53–76 (2005)

    Article  Google Scholar 

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Acknowledgements

We thank museums, institutions and individuals that made specimens available for this study (full list is available in Supplementary Information). Funding was provided by the National Science Foundation, Denver Museum, the University of Washington (G.P.W. and P.D.S.), the Australian Research Council, Monash University (A.R.E.), the Academy of Finland (A.R.E., M.F. and J.J.) and the EU SYNTHESYS program (project GB-TAF-4779) (I.J.C.).

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Contributions

G.P.W., A.R.E., J.J. and M.F. designed the study. G.P.W., A.R.E, I.J.C. and P.D.S. collected and analysed the data. G.P.W., A.R.E. and J.J. wrote the manuscript. G.P.W., A.R.E., I.J.C., P.D.S., M.F. and J.J. discussed results and commented on the manuscript at all stages.

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Correspondence to Gregory P. Wilson.

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The authors declare no competing financial interests.

Additional information

The three-dimensional scans for this study are deposited in the MorphoBrowser database (http://morphobrowser.biocenter.helsinki.fi/).

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Supplementary Information

This file contains Supplementary Text, Supplementary Figures 1-10, Supplementary Tables 1-7 and additional references. (PDF 3070 kb)

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Wilson, G., Evans, A., Corfe, I. et al. Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature 483, 457–460 (2012). https://doi.org/10.1038/nature10880

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