Phenotypic and dynamical transitions in model genetic networks II. Application to the evolution of segmentation mechanisms

Authors

  • I. Salazar-Ciudad,

    1. Complex Systems Research Group, Department of Physics, (FEN) Universitat Politecnica de Catalunya. Campus Nord,
      Modul B5 08034 Barcelona, Spain;
    2. Departament de Genètica, Facultat de Biologia, Universitat de Barcelona,
      Diagonal 645, 08028 Barcelona, Spain; and
    Search for more papers by this author
  • R. V. Solé,

    1. Departament de Genètica, Facultat de Biologia, Universitat de Barcelona,
      Diagonal 645, 08028 Barcelona, Spain; and
    Search for more papers by this author
  • S. A. Newman

    Corresponding author
    1. Department of Cell Biology and Anatomy, Basic Science Building,
      New York Medical College, Valhalla, NY 10595, USA
    Search for more papers by this author

*Author for correspondence (email: newman@nymc.edu)

Abstract

SUMMARY Knowledge of the genetic control of segmentation in Drosophila has made insect segmentation a paradigmatic case in the study of the evolution of developmental mechanisms. In Drosophila, the patterns of expression of segmentation genes are established simultaneously in all segments by a complex set of interactions between transcriptional factors that diffuse in a syncytium occupying the whole embryo. Such mechanisms cannot act in short germ-band insects where segments appear sequentially from a cellularized posterior proliferative zone. Here, we compare mechanisms of segmentation in different organisms and discuss how the transition between the different types of segmentation can be explained by small and progressive changes in the underlying gene networks. The recent discovery of a temporal oscillation in expression during somitogenesis of vertebrate homologs of the pair-rule gene hairy enhances the plausibility of an earlier proposal that the evolutionary origin of both the short- and long germ-band modes of segmentation was an oscillatory genetic network (Newman 1993). An implication of this scenario is that the self-organizing, pattern-forming system embodied in an oscillatory network operating in the context of a syncytium (i.e., a reaction-diffusion system)—which is hypothesized to have originated the simultaneous mode of segmentation—must have been replaced by the genetic hierarchy seen in modern-day Drosophila over the course of evolution. As demonstrated by the simulations in the accompanying article, the tendency for “emergent” genetic networks, associated with self-organizing processes, to be replaced through natural selection with hierarchical networks is discussed in relation to the evolution of segmentation.

Ancillary