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A new heart for a new head in vertebrate cardiopharyngeal evolution

Nature volume 520, pages 466–473 (2015)Cite this article

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Abstract

It has been more than 30 years since the publication of the new head hypothesis, which proposed that the vertebrate head is an evolutionary novelty resulting from the emergence of neural crest and cranial placodes. Neural crest generates the skull and associated connective tissues, whereas placodes produce sensory organs. However, neither crest nor placodes produce head muscles, which are a crucial component of the complex vertebrate head. We discuss emerging evidence for a surprising link between the evolution of head muscles and chambered hearts — both systems arise from a common pool of mesoderm progenitor cells within the cardiopharyngeal field of vertebrate embryos. We consider the origin of this field in non-vertebrate chordates and its evolution in vertebrates.

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Figure 1: The striking heterogeneity of the human head and heart musculature.
Figure 2: An evolutionarily conserved cardiopharyngeal ontogenetic motif.
Figure 3: Some of the synapomorphies of the Chordata and its subgroups, according to our own data and review of the literature.
Figure 4: Homology hypotheses of placodes and branchiomeric muscles within chordates.

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Acknowledgements

We thank T. Miyashita and F. Razy-Krajka for their detailed reviews of the manuscript. We are thankful to the Dean of Howard University (HU) College of Medicine, M. Johnson, and the Chair of HU Department of Anatomy, D. Orlic, for helping to organize, financially and logistically, the First Evo-Devo Meeting On Heart and Head Muscles at HU (May, 2014) that led to the publication of this Review. We also thank the other participants at the workshop: A. Kahana, P. Okkema, A. Vincent, T. Hirasawa, S. Tajbakhsh, S. Dietrich and R. Knight. L.C. is supported by National Institutes of Health (NIH)/National Institute of General Medical Sciences (NIGMS) grant R01GM096032 and NIH/National Heart, Lung and Blood Instiute (NHLBI) grant R01HL108643, E.T. by the European Research Council and Israel Science Foundation, R.D. and J.Z. by HU College of Medicine, R.G.K. by Inserm, the Agence Nationale pour la Recherche, Association Française contre les Myopathies and Fondation pour la Recherche Médicale, and M.L. by NIH grant NS076542.

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Authors and Affiliations

  1. Department of Anatomy, Howard University College of Medicine, 20059, Washington DC, USA

    Rui Diogo, Janine M. Ziermann & Julia L. Molnar

  2. Aix Marseille Université, Centre National de la Recherche Scientifique, Institut de Biologie du Développement de Marseille UMR 7288, Marseille, 13288, France

    Robert G. Kelly

  3. Department of Biology, Center for Developmental Genetics, New York University, 10003, New York, USA

    Lionel Christiaen

  4. Department of Molecular and Cell Biology, University of California at Berkeley, California 94720, USA.,

    Michael Levine

  5. Department of Biomedical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, 14853, New York, USA

    Drew M. Noden

  6. Department of Biological Regulation, Weizmann Institute of Science, Rehovot, 76100, Israel

    Eldad Tzahor

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  1. Rui Diogo
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Correspondence to Rui Diogo, Robert G. Kelly, Lionel Christiaen or Eldad Tzahor.

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Diogo, R., Kelly, R., Christiaen, L. et al. A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature 520, 466–473 (2015). https://doi.org/10.1038/nature14435

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