BioSystems 56 2000 1 – 11
Connectance in Sorghum development: beyond the genotype – phenotype duality
G.N. Amzallag
Department of Plant Sciences, The Hebrew Uni6ersity of Jerusalem, Jerusalem
91904
, Israel Received 15 September 1998; received in revised form 20 October 1999; accepted 8 November 1999
Abstract
Connectance, the level of linkage between organs, was measured in different lines of Sorghum bicolor during their reproductive development. It was compared with expression of characters, their level of variability and their
heritability. A negative relationship is observed between connectance and heritability. Further results indicate that connectance does not simply introduce a noise factor in expression of a pre-existing information, but that it is directly
involved in phenotypic expression and plasticity. Connectance appears as partly determined by the nature and dynamics of the network of relationships. It is concluded that the phenotype is not restricted to the deterministic
expression of a pre-existing program, the genotype. Morphogenesis also involves another dimension, self-organized, which confers reliability, stability and adaptability to the developmental processes. The complex interactions between
these two dimensions and their evolutionary consequences are discussed. © 2000 Elsevier Science Ireland Ltd. All rights reserved.
Keywords
:
Morphogenesis; Connectance; Self-organization; Developmental network; Adaptability; Phenotypic plasticity www.elsevier.comlocatebiosystems
1. Introduction
It is generally assumed that the phenotype re- sults from a deterministic, though complex, ex-
pression of
a pre-existing
information, the
genotype. Indeed, a direct relationship between genotype and phenotype may be observed in adult
organisms. However, the control of developmen- tal processes is not directly related to the gene-en-
coded
information. For
example, discrete
morphological patterns are represented at a defined frequency within a population, and those
independently of the genetic variation encoun- tered Alberch, 1980. From these observations,
Alberch 1980 concluded that ‘‘The complexity of interactions during development renders the anal-
ysis of patterns of morphological evolution im- possible to reduce to a problem of change in gene
frequency’’. This opinion was confirmed by stud- ies in quantitative genetics in which normal distri-
butions of characters are observed independently of the frequency distribution of specific alleles
Barton and Turelli, 1989.
Complex models including multiple sets of al- lele interactions were proposed in order to explain
this feature in terms of genotypephenotype dual-
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PII: S 0 3 0 3 - 2 6 4 7 0 0 0 0 0 6 8 - X
ity. As emphasized by Lewontin 1974, this mode of interpretation involving a cumulative effect of
specific alleles ‘‘comes from a general Cartesian world view that things can be broken down into
parts without losing any essential information…’’ Lewontin, 1974.
Development is extremely extended in plants, as compared with animals. This may be the reason
why, in plants, most of the morphological, behav- ioral and physiological differences among individ-
ual do not ‘mendelize’ Sultan, 1992, and why the plasticity observed during development is so
adaptive Bradshaw, 1965; Moran et al., 1981; Sultan, 1987. Accordingly, there must be another
central factor, generated by the de6elopment itself, which enables harmonized achievement of the de-
velopment in spite of genetic, developmental or environmental perturbations. Such a property has
been termed canalization Waddington, 1942, equifinality von Bertalanffy, 1950, correcti6e
pleiotropy Warburton, 1955, or adapti6e deter- minism Seligmann and Amzallag, 1995. Its in-
volvement
does not
imply any
vitalistic explanation, but only to consider living organisms
in development as open systems with a sponta- neous tendency to reach the minimal free-energy
status Prigogine and Wiame, 1946. More re- cently, Conrad 1990 suggested the existence of
thermodynamic
basins of
attraction sponta-
neously emerging in the phenotypic landscape, which are involved in a structural increase in
complexity and adaptive responses during devel- opment. These considerations point to the emer-
gence of a self-organized dimension during development Conrad, 1983; Ito and Gunji, 1997;
Hiett, 1999. Recently, experimental measure- ments have confirmed the self-organizing nature
of specific transition phases in plant development Amzallag, 1999a,b.
Theoretical considerations suggest that emer- gence of the self-organization dimension in devel-
opment results from changes in the level of self-association Chauvet, 1993. On the other
hand, it was observed that, in Sorghum bicolor, the level of linkage between different organs is not
constant during development, and that sudden modifications occurred specifically during the
transition phases Amzallag, 1999a. More gener- ally, Trewavas and Malho 1997 have suggested
that the phenotypic dimension is generated by the network of cell-to-cell, and organ-to-organ rela-
tionships. All these considerations indicate that the level of linkage during development may be
both the result and the condition for emergence of self-organizing processes. The aim of the present
study is to investigate whether connectance, a quantification of the network of relationships
within the developing organism, is an expression of the self-organized dimension of development.
This hypothesis is tested here through analysis of connectance and its relationship with expression
and transmissibility of reproductive characters in S. bicolor.
2. Materials and methods
