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Body Plan Identity: A Mechanistic Model

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We surmise that the commonality of anatomy among groups sharing a body plan is not merely an incidental sharing of descriptive features, but rather, that those features are the component parts of a deeply integrated shared pattern of development.

—Raff, R. A. (1996). The shape of life: Genes, development, and the evolution of animal form (p. 31). University of Chicago Press.

Abstract

A body plan is a stable configuration of characters for a major taxonomic group, such as chordates or arthropods. Despite widespread casual reliance on the concept for guiding comparisons within and between groups, the nature of body plans as well as the biological causes underlying their evolution have remained elusive. This paper proposes an abstract mechanistic model of body plan identity. We hypothesize that body plans are an evolutionary phenomenon that only applies to a relatively small subset of major clades, rather than being associated with each and every so-called “phylum.” Body plans arise in evolution by stepwise accretion, and require a level of developmental complexity that is only found in some animal clades. Further, we suggest that, parallel to the developmental mechanisms controlling character identity, there are “body plan identity mechanisms” (BpIMs) that maintain entire configurations of characters while possessing a mechanistic architecture that is itself stable and traceable through evolutionary change. These BpIMs, we suggest, are entrenched intercellular signaling networks operating between transient embryonic structures that are destined to differentiate into distinct individualized characters. The activity of a BpIM results in a transient long-range integration of the embryo that is highly sensitive to genetic and environmental perturbations, and that can be detected morphologically as a conserved phylotypic stage. This model is illustrated with detailed interpretations of the notochord signaling system and the segment polarity network as candidate BpIMs in vertebrates and arthropods, respectively. We conclude by contrasting the proposed developmental-mechanistic conception of body plans with the phylogenetic notion of ground plans, and sketch the general outlines of an empirical research program on body plan evolution.

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Notes

  1. We do not distinguish between concepts of body plan and Bauplan, which we understand to be equivalent.

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Acknowledgements

GPW gratefully acknowledges the financial support of the John Templeton Foundation (Grant No. 61329). The opinions expressed in this paper are those of the authors and not those of the JTF. JD thanks the Research Foundation—Flanders (FWO) for financial support (Grant Nos. 41277 and 88559).

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Authors and Affiliations

  1. Institute of Philosophy, KU Leuven, Leuven, Belgium

    James DiFrisco

  2. Department of Ecology and Evolutionary Biology, Yale University, New Haven, USA

    Günter P. Wagner

  3. Yale Systems Biology Institute, West Haven, USA

    Günter P. Wagner

  4. Department of Obstetrics, Gynecology and Reproductive Sciences, Yale Medical School, New Haven, USA

    Günter P. Wagner

  5. Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA

    Günter P. Wagner

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  1. James DiFrisco
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  2. Günter P. Wagner
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Correspondence to Günter P. Wagner.

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DiFrisco, J., Wagner, G.P. Body Plan Identity: A Mechanistic Model. Evol Biol 49, 123–141 (2022). https://doi.org/10.1007/s11692-022-09567-z

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  • DOI: https://doi.org/10.1007/s11692-022-09567-z

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