Developing Organisms as Self-Organizing Fields

Abstract

The way in which parts are related to wholes is crucial to any theory of self-organization, since it is necessary to know what is being organized and what collective properties they reveal. The analytic tradition of science uses an atomistic description of this relationship: parts (“atoms”) are assumed to be primary and the whole is generated by their interaction. This approach dominates modern embryology and evolutionary biology. However, there is an alternative view that is very useful in understanding complex order, which is the structuralist tradition: a whole entity is defined by invariant relations within which parts emerge and behave in accordance with transformational principles. Evidence that the constraints determining biological form arise from organizational levels other than the genome and gene products emphasizes the primacy of morphogenetic principles at the level of the organism, and the inadequacy of atomistic theories on which the concept of the genetic program is based.

Many field theories in physics illustrate structuralist principles in that descriptions of global order are primary to the analysis (e.g., the Pauli exclusion principle, or Bell’s theorem and nonlocal connectedness), so that the behavior of the system is not reducible to interactions of “atomic” constituents such as electrons or photons. In biology, field concepts have been used for many years to describe the behavior of developing embryos, which reveal high-level order and systematic spatial transformations suggestive of principles of global organization. An application of a particularly simple type of field theory to the earliest stage of embryonic development in many species, involving the use of harmonic functions to describe the systematic transformations of the fertilized egg through cleavage stages, illustrates the general principles as they apply to embryogenesis. The specific set of harmonic functions describing the cleavage planes are specified by selection rules which are related to particular aspects of embryonic organization, some arising from properties of the whole and some from properties of parts. This type of field analysis is then extended to a qualitative description of how the next stage of embryogenesis, gastrulation, could emerge from the conditions resulting from cleavage. Such field descriptions allow for comparisons of morphogenetic principles between unicellular and multicellular organisms, despite the fact that at one level of analysis their “parts” appear to be different. This illustrates the principles of a structuralist analysis, which leads one to seek organismic homologies at the level of primary generative principles (deep structure) such as those defining field properties, and not in terms of genetic composition or historical relatedness. —The Editor