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Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size

Author

Listed:
  • Daisuke Koyabu

    (Palaeontological Institute and Museum, University of Zürich
    The University Museum, The University of Tokyo)

  • Ingmar Werneburg

    (Palaeontological Institute and Museum, University of Zürich)

  • Naoki Morimoto

    (Anthropological Institute and Museum, University of Zürich)

  • Christoph P. E. Zollikofer

    (Anthropological Institute and Museum, University of Zürich)

  • Analia M. Forasiepi

    (Palaeontological Institute and Museum, University of Zürich
    Ianigla, CCT-Mendoza, CONICET, Avda. Ruiz Leal s/n)

  • Hideki Endo

    (The University Museum, The University of Tokyo)

  • Junpei Kimura

    (College of Veterinary Medicine, Seoul National University)

  • Satoshi D. Ohdachi

    (Institute of Low Temperature Science, Hokkaido University)

  • Nguyen Truong Son

    (Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology)

  • Marcelo R. Sánchez-Villagra

    (Palaeontological Institute and Museum, University of Zürich)

Abstract

The multiple skeletal components of the skull originate asynchronously and their developmental schedule varies across amniotes. Here we present the embryonic ossification sequence of 134 species, covering all major groups of mammals and their close relatives. This comprehensive data set allows reconstruction of the heterochronic and modular evolution of the skull and the condition of the last common ancestor of mammals. We show that the mode of ossification (dermal or endochondral) unites bones into integrated evolutionary modules of heterochronic changes and imposes evolutionary constraints on cranial heterochrony. However, some skull-roof bones, such as the supraoccipital, exhibit evolutionary degrees of freedom in these constraints. Ossification timing of the neurocranium was considerably accelerated during the origin of mammals. Furthermore, association between developmental timing of the supraoccipital and brain size was identified among amniotes. We argue that cranial heterochrony in mammals has occurred in concert with encephalization but within a conserved modular organization.

Suggested Citation

  • Daisuke Koyabu & Ingmar Werneburg & Naoki Morimoto & Christoph P. E. Zollikofer & Analia M. Forasiepi & Hideki Endo & Junpei Kimura & Satoshi D. Ohdachi & Nguyen Truong Son & Marcelo R. Sánchez-Villag, 2014. "Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size," Nature Communications, Nature, vol. 5(1), pages 1-9, May.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms4625
    DOI: 10.1038/ncomms4625
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    Cited by:

    1. Jasmien Roosenboom & Myoung Keun Lee & Jacqueline T Hecht & Carrie L Heike & George L Wehby & Kaare Christensen & Eleanor Feingold & Mary L Marazita & A Murat Maga & John R Shaffer & Seth M Weinberg, 2018. "Mapping genetic variants for cranial vault shape in humans," PLOS ONE, Public Library of Science, vol. 13(4), pages 1-14, April.

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