A field description of the cleavage process in embryogenesis

Goodwin, Brian C.; Trainor, L. E. H.

doi:10.1016/0022-5193(80)90270-2

Cited by 70 publications

(15 citation statements)

References 3 publications

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“…For ''pure functionalists,'' phylogenetic patterns are constraints that may prevent organisms from reaching optimal adaptation to current conditions. Finally, ''structuralists'' put the accent on the self-organizing morphogenetic properties of development (Goodwin and Trainor 1980;Seilacher 1991;Kauffman 1993;Hickman 2004). These three intellectual frameworks, although useful to answer some questions, are ''reality bites'' which are far from a desirable integrative (holistic) approach.…”

Section: Introductionmentioning

confidence: 97%

Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes

Cubo

Legendre

Ricqlès

et al. 2008

Evolution and Development

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The biological features observed in every living organism are the outcome of three sets of factors: historical (inherited by homology), functional (biological adaptation), and structural (properties inherent to the materials with which organs are constructed, and the morphogenetic rules by which they grow). Integrating them should bring satisfactory causal explanations of empirical data. However, little progress has been accomplished in practice toward this goal, because a methodologically efficient tool was lacking. Here we use a new statistical method of variation partitioning to analyze bone growth in amniotes. (1) Historical component. The variation of bone growth rates contains a significant phylogenetic signal, suggesting that the observed patterns are partly the outcome of shared ancestry. (2) Functional causation. High growth rates, although energy costly, may be adaptive (i.e., they may increase survival rates) in taxa showing short growth periods (e.g., birds). In ectothermic amniotes, low resting metabolic rates may limit the maximum possible growth rates. (3) Structural constraint. Whereas soft tissues grow through a multiplicative process, growth of mineralized tissues is accretionary (additive, i.e., mineralization fronts occur only at free surfaces). Bone growth of many amniotes partially circumvents this constraint: it is achieved not only at the external surface of the bone shaft, but also within cavities included in the bone cortex as it grows centrifugally. Our approach contributes to the unification of historicism, functionalism, and structuralism toward a more integrated evolutionary biology.

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Section: Introductionmentioning

confidence: 97%

Phylogenetic, functional, and structural components of variation in bone growth rate of amniotes

Cubo

Legendre

Ricqlès

et al. 2008

Evolution and Development

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“…Preliminary essays in this direction have been published (Goodwin, 1980;Goodwin andTrainor, 1980, 1985). This approach will now be illustrated by an analysis of the earliest stage of amphibian embryogenesis, following the treatment of Goodwin and Trainor (1980), and then certain conclusions regarding self-organization in biology will be drawn.…”

Section: Organisms As Fieldsmentioning

confidence: 99%

Developing Organisms as Self-Organizing Fields

Goodwin

1987

Self-Organizing Systems

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9The 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 modem 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 offield 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

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“…While it is true that biology has produced some facts which are consistent with such a view, it should be reemphasised that such facts in no way necessitate it. There are no a priori grounds for supposing that organisms cannot be selforganising entities, "decentered structures," and, indeed, Kauffman [36] has clearly demonstrated that orderly behaviour in time can emerge in a network as a consequence of its total relational structure; organisation in space can be similarly treated by the use of field descriptions [37][38][39].…”

Section: The Structuralist View Of the Biological Domainmentioning

confidence: 99%

“…What is now required is to transform this metaphor into a specific theory. Attempts to do this are presented elsewhere [37][38][39].…”

Section: The Structuralist View Of the Biological Domainmentioning

confidence: 99%