Dynamical patterning modules: a "pattern language" for development and evolution of multicellular form

Int J Dev Biol. 2009;53(5-6):693-705. doi: 10.1387/ijdb.072481sn.

Abstract

This article considers the role played by a core set of "dynamical patterning modules" (DPMs) in the origination, development and evolution of complex organisms. These consist of the products of a subset of the genes of what has come to be known as the "developmental-genetic toolkit" in association with physical processes they mobilize. The physical processes are those characteristic of chemically and mechanically excitable mesoscopic systems like cell aggregates: cohesion, viscoelasticity, diffusion, spatiotemporal heterogeneity based on activator-inhibitor interaction, and multistable and oscillatory dynamics. We focus on the emergence of the Metazoa, and show how toolkit gene products and pathways that pre-existed the metazoans acquired novel morphogenetic functions simply by virtue of the change in scale and context inherent to multicellularity. We propose that DPMs, acting singly and in combination with each other, constitute a "pattern language" capable of generating all metazoan body plans and organ forms. This concept implies that the multicellular organisms of the late Precambrian-early Cambrian were phenotypically plastic, fluently exploring morphospace in a fashion decoupled from both function-based selection and genotypic change. The relatively stable developmental trajectories and morphological phenotypes of modern organisms, then, are considered to be products of stabilizing selection. This perspective solves the apparent "molecular homology-analogy paradox," whereby widely divergent modern animal types utilize the same molecular toolkit during development, but it does so by inverting the neo-Darwinian principle that phenotypic disparity was generated over long periods of time in concert with, and in proportion to genotypic change.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Review

MeSH terms

  • Animals
  • Biological Evolution
  • Body Patterning*
  • Cell Adhesion
  • Developmental Biology / methods
  • Elasticity
  • Epithelium / pathology
  • Mesoderm / pathology
  • Models, Biological*
  • Morphogenesis
  • Oscillometry
  • Phenotype
  • Time Factors