Article

The delayed rise of present-day mammals

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Abstract

Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic ‘fuses’ leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today’s mammals.

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Acknowledgements

D. Wong and A. Mooers provided their unpublished supertree of Geomyoidea. T. Barraclough, J. Bielby, N. Cooper, T. Coulson, M. Crawley, J. Davies, S. Fritz, N. Isaac, A. Lister, K. Lyons, G. Mace, S. Meiri, D. Orme, G. Thomas and N. Toomey all provided support and/or suggestions to improve the manuscript. Funding came from the NCEAS Phylogeny and Conservation Working Group; the BMBF; a DFG Heisenberg Scholarship; NERC studentships and grants; the Leverhulme Trust; the NSF; an Earth Institute Fellowship; and a CIPRES postdoctoral fellowship.

Author Contributions O.R.P.B.-E. developed data and computer protocols underlying the supertree and dating analyses, contributed to or performed many of the supertree analyses, generated the molecular data set and dated the supertree, and wrote major portions of the manuscript; M.C. helped develop data protocols, contributed source trees and performed many of the intraordinal supertree analyses, and helped write parts of the manuscript; K.E.J. contributed source trees, developed data protocols, collected the fossil database and performed associated analysis; R.D.E.M. provided relevant palaeontological information and first appearance dates of major clades, and collected the fossil database and performed associated analysis; R.M.D.B. contributed to and performed selected supertree analyses, and provided relevant palaeontological information; R.G. developed protocols for and performed supertree construction and macroevolutionary analyses, and contributed to the writing of the manuscript; S.A.P. developed data protocols, collected source trees for and built the cetartiodactyl and perissodactyl portions of the supertree; R.A.V. provided source trees for Primates; J.L.G. provided source trees and ideas for comparative tests; and A.P. developed, conceived and performed the macroevolutionary analyses, wrote the corresponding sections of the manuscript and developed data protocols. All authors provided comments on the manuscript.

Author information

Author notes

    • Olaf R. P. Bininda-Emonds
    •  & Marcel Cardillo

    Present addresses: Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Friedrich-Schiller-Universität Jena, 07743 Jena, Germany (O.R.P.B.-E.); Centre for Macroevolution and Macroecology, School of Botany and Zoology, Australian National University, Canberra 0200, Australia (M.C.).

Affiliations

  1. Lehrstuhl für Tierzucht, Technical University of Munich, 85354 Freising-Weihenstephan, Germany

    • Olaf R. P. Bininda-Emonds
  2. Division of Biology, and,

    • Marcel Cardillo
    •  & Andy Purvis
  3. NERC Centre for Population Biology, Imperial College, Silwood Park campus, Ascot SL5 7PY, UK

    • Andy Purvis
  4. Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK

    • Kate E. Jones
  5. Division of Vertebrate Zoology, American Museum of Natural History, New York, New York 10024, USA

    • Ross D. E. MacPhee
  6. School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales 2052, Australia

    • Robin M. D. Beck
  7. Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK

    • Richard Grenyer
  8. National Evolutionary Synthesis Center (NESCent), Durham, North Carolina 27705, USA

    • Samantha A. Price
  9. Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada

    • Rutger A. Vos
  10. Institute of Ecology, University of Georgia, Athens, Georgia 30602, USA

    • John L. Gittleman

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Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Corresponding author

Correspondence to Olaf R. P. Bininda-Emonds.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Methods describing the procedures used in the paper in greater detail, Supplementary Figures 2–4 with Legends, Supplementary Tables 1, 3, and 4, Supplementary Results and additional references.

  2. 2.

    Supplementary Information

    This file was amended on 13 November 2008 because the authors discovered a bug in the Perl script relDate v.2.2 that was used in part to date the nodes in the species-level mammalian supertree presented and analysed in their Article and original Supplementary Information; see the related Corrigendum (nature07347).

Text files

  1. 1.

    Supplementary Figure 1

    This file represents Supplementary Figure 1 and contains three alternatively dated versions of the mammalian supertree (all in nexus format), providing the best estimates of the divergence times and the upper and lower confidence intervals on these dates.

  2. 2.

    Supplementary Figure 1

    This file was amended on 13 November 2008 because the authors discovered a bug in the Perl script relDate v.2.2 that was used in part to date the nodes in the species-level mammalian supertree presented and analysed in their Article and original Supplementary Information; see the related Corrigendum (nature07347).

Excel files

  1. 1.

    Supplementary Table 2

    This file represents Supplementary Table 2 and presents a summary of the taxonomic identity and divergence time estimates for each node on the supertree.

  2. 2.

    Supplementary Table 2

    This file was amended on 13 November 2008 because the authors discovered a bug in the Perl script relDate v.2.2 that was used in part to date the nodes in the species-level mammalian supertree presented and analysed in their Article and original Supplementary Information; see the related Corrigendum (nature07347).

  3. 3.

    Supplementary Table 5

    This file represents Supplementary Table 5 and summarizes the occurrence of mammalian genera in 11subepochs from the Late Triassic until Late Eocene using data from the Unitaxon database.