A Model for Development and Evolution of Complex Morphological Structures

Abstract

How 'complex' or composite morphological structures like the mammalian craniomandibular region arise during development and how they are altered during evolution are two major unresolved questions in biology. Herein, we have described a model for the development and evolution of complex morphological structures. The model assumes that natural selection acts upon an array of phenotypes generated by variation in a variety of underlying genetic and epigenetic controlling factors. Selection refines the integration of the various morphogenetic components during ontogeny in order to produce a functioning structure and to adapt the organisms to differing patterns of environmental heterogeneity. The model was applied to the development and evolution of the mammalian mandible (which is used as a paradigm of complex morphological structures). The embryology of the mandible was examined in detail in order to identify the fundamental developmental units which are necessary to assemble the final morphological structure. The model is quite general since equivalent units exist for the development of many other biological structures. This model could be applied to many other developing morphological structures as well as other groups of organisms. For example, it can be applied to cell parameters during Drosophila development (Atchley, 1987). The model as discussed in this paper assumes that morphological changes in the mandible result from evolutionary changes in its underlying developmental units. The developmental units relate to characteristics of cellular condensations which are produced from the differentiation of embryonic neural crest cells. The developmental units include: the number of stem cells in preskeletal condensations (n), the time of initiation of condensation formation (t), the fraction of cells that is mitotically active within a condensation (f), the rate of division of these cells (r), and their rate of cell death (d). These units and their derivative structures are discussed in terms of types of tissue differentiation (chondrogenesis, osteogenesis, primary/secondary osteogenesis, intramembranous/endochondral ossification) and growth properties of major morphological regions of the mandible. Variation in these five units provides the developmental basis for ontogenetic and phylogenetic modification of mandibular morphology. We have discussed how these developmental units are influenced by (a) the cell lineage from which they arise, (b) epithelial-mesenchymal (inductive tissue) interactions, (c) regulation of cell differentiation, and (d) extrinsic factors such as muscles, teeth and hormones. Evidence was provided that variation in mandibular morphology is heritable, subject to modification by natural selection, and that divergence among different genetic stocks has apparently occurred through changes in these developmental units and their derivative structures.(ABSTRACT TRUNCATED AT 400 WORDS)

Genetic and developmental basis of cichlid trophic diversity

“…In mice lacking pax9, jaw length is relatively unaffected, however, the coronoid process is missing (Peters et al, 1998). This is a very specific defect, probably related to the role of pax-9 in promoting mesenchymal condensation (Peters et al, 1999) and the observation that the coronoid process develops from a distinct CNC condensation (Atchley and Hall, 1991). In both mice and zebrafish, loss of bapx1 activity leads to a loss of the retroarticular process (Miller et al, 2003;Wilson and Tucker, 2004).…”

Speciation through the lens of biomechanics: locomotion, prey capture and reproductive isolation

“…The action of selection on the developmentalgenetic architecture underlying functionally correlated traits relatively stronger covariation between such traits as a unit, in comparison to the rest of the phenotype [73,74]. Covariation is also influenced by drift and gene flow [75,76], and can constrain the range of possible phenotypes available for selection [77,78] and bias the direction of evolution [79]. Alternatively, patterns of phenotypic covariation can facilitate adaptive change without compromising function [74,[80][81][82].…”

Mathematical Analysis of Mandibular Morphogenesis by Micro‐CT‐Based Mouse and Alizarin Red S‐Stained‐Based Human Studies During Development

“…By the mathematical analysis used in the present study, we can compare the shape of the mandible between the individuals, but not the size. The emphasis on the shapes of biological structures is based on the observation that, of the two components of form (size and shape), shape is multidimensional and provides a good deal of information about the historical (evolutionary) processes responsible for the observed diversity (Rohlf and Bookstein, 1987;Smith and Patton, 1988;Patton and Smith, 1990;Atchley and Hall, 1991;Atchley et al, 1992;Raff, 1996).…”

“…The mandible originates from cells of the neural crest that migrate to the first mandibular arch and form the embryonic mesenchyme, which later develops into skeletal, dental, and connective tissues. The mesenchymal cells aggregate and produce condensations before undergoing differentiation to produce the morphogenetic components of the mandible (Atchley and Hall, 1991). The mandible consists of two symmetrical halves (right and left), each formed by a dentary bone with four morphogenetic regions: the mandibular body (ramus) and three processes (coronoid, condylar, and angular).…”