The role of self-organization in developmental evolution

Abstract

In developmental and evolutionary biology, particular emphasis has been given to the relationship between transcription factors and the cognate cis-regulatory elements of their target genes. These constitute the gene regulatory networks that control expression and are assumed to causally determine the formation of structures and body plans. Comparative analysis has, however, established a broad sequence homology among species that nonetheless display quite different anatomies. Transgenic experiments have also confirmed that many developmentally important elements are, in fact, functionally interchangeable. Although dependent upon the appropriate degree of gene expression, the actual construction of specific structures appears not directly linked to the functions of gene products alone. Instead, the self-formation of complex patterns, due in large part to epigenetic and non-genetic determinants, remains a persisting theme in the study of ontogeny and regenerative medicine. Recent evidence indeed points to the existence of a self-organizing process, operating through a set of intrinsic rules and forces, which imposes coordination and a holistic order upon cells and tissue. This has been repeatedly demonstrated in experiments on regeneration as well as in the autonomous formation of structures in vitro. The process cannot be wholly attributed to the functional outcome of protein-protein interactions or to concentration gradients of diffusible chemicals. This phenomenon is examined here along with some of the methodological and theoretical approaches that are now used in understanding the causal basis for self-organization in development and its evolution.

Reconsidering regeneration in metazoans: an evo-devo approach

“…The cellular and molecular mechanisms occurring during regeneration can be treated in the same manner as ontogenetic phenomena, and therefore conceptual approaches similar to those employed in comparative and evolutionary developmental biology can be applied. If we accept such parallelism, regeneration is faced with the same set of problems and challenges as evolutionary and developmental biology, for instance the complexities of the genotype-phenotype map, i.e., the degree of phenotypic diversity among metazoans, yet relatively conserved sequence repertoires (Wagner and Zhang, 2011;Bozorgmehr, 2014). Regenerative events do not escape from such developmental and evolutionary dynamics, and concepts like pleiotropy, exaptation, developmental constraints and variational properties can provide a useful framework to better understand the phenomena of regeneration and their evolution.…”

Adaptive self‐organization in the embryo: its importance to adult anatomy and to tissue engineering

“…Commentators such as Bozorgmehr (2014) have pointed out that the most interesting and effective approaches to synthetic development would be those that produce cell behaviours leading to self-organization and the emergence of coherent large-scale structures. Some progress has been made in this direction by constructing a patterning system in which randomly mixed cells organize themselves into patches somewhat reminiscent of animal coat markings (Cachat et al 2016).…”

“…A solution to the paradox, a solution that has been written about many times before (Turing, ; Meinhardt & Gierer, ; Davies, ; Bozorgmehr, ), although it has not succeeded in expunging the idea of anatomical features being under direct genetic control (‘a gene for’ a specific anatomical feature), is to view anatomy as emerging from a complex interaction of cells that use communication to organize themselves according to the conditions in which they actually find themselves. Understanding the basis of this adaptive self‐organization is therefore critical for understanding development, for understanding how variation arises, and for explaining how it can do so harmlessly.…”

Shared rules of development predict patterns of evolution in vertebrate segmentation

“…While morphogenesis of each of these organ systems utilizes similar developmental processes of 'outgrowth and segmentation' [7][8][9] , a lack of genetic and structural homology among them has led to the presumption that different developmental principles must apply to each system. Commonalities in regulatory 'logic' may predict similar underlying 'rules' of variation even when the underlying identity of cellular or molecular players differs [10][11][12][13] . One such model, the inhibitory cascade (IC) 14 , is particularly promising for understanding iterative segmentation in a range of disparate organ systems.…”