4.2 Article

Body Plan Identity: A Mechanistic Model

Journal

EVOLUTIONARY BIOLOGY
Volume 49, Issue 2, Pages 123-141

Publisher

SPRINGER
DOI: 10.1007/s11692-022-09567-z

Keywords

Body plan; Burden; Phylotypic stage; Hourglass model; Notochord; Segment polarity

Funding

  1. John Templeton Foundation [61329]
  2. Research Foundation-Flanders (FWO) [41277, 88559]

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This paper proposes an abstract mechanistic model of body plan identity. Body plans are an evolutionary phenomenon that only applies to a relatively small subset of major clades. Body plan identity mechanisms (BpIMs) maintain entire configurations of characters while possessing a stable and traceable mechanistic architecture. These BpIMs are intercellular signaling networks operating between transient embryonic structures.
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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