Is There a Link Between Changes in the Vertebral “hoxcode” and the Shape of Vertebrae? A Quantitative Study of Shape Change in the Cervical Vertebral Column of Mice

doi:10.1006/jtbi.1996.0204

Journal of Theoretical Biology

Volume 183, Issue 1, 7 November 1996, Pages 89-93

https://doi.org/10.1006/jtbi.1996.0204 Get rights and content

Abstract

Homeobox (hox) genes are of considerable importance in the formation of the body axis of invertebrates and vertebrates. The postulation of ahox-code (i.e. the simultaneous activity of a certain subset ofhoxgenes) for structures at different metameric levels and which differ from each other in shape suggests a relationship betweenhox-code and shape, which is reinforced by the possibility of homeotic transformation when thehox-code is changed experimentally. This paper considers the possible nature of such a relationship between thehoxgenes governing vertebral formation in the upper part of the mouse vertebral column and the shape of the adult vertebrae formed in this region.

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Citation Excerpt :
The number of vertebrae in the vertebral column is regulated by the expression of the Hox genes, and those of the paralog groups 4 and 5 control the organization of the cervical region (Kessel and Gruss, 1991; Burke et al., 1995; Galis, 1999a; Wellik and Capecchi, 2003). In mammals, almost all species present a fixed number of seven cervical vertebrae (Bateson, 1894; Johnson and O'Higgins, 1996; Galis, 1999b; Narita and Kuratani, 2005; Varela-Lasheras et al., 2011; Buchholtz, 2014; Böhmer, 2017; Böhmer et al., 2018), which, at the same time, are internally organized into three functional and developmental modules: upper (C1–C2), middle (C3–C5), and lower cervical (C6–C7; Arnold et al., 2016; Randau et al., 2017). Other studies proposed a slightly different subdivision of the cervical spine, which includes either the cranial base (CB) as part of the upper module (i.e., CB–C1) or the cranium and thoracic spine for some species (Arnold et al., 2017a; Villamil, 2018).
The analysis of patterns of integration is crucial for the reconstruction and understanding of how morphological changes occur in a taxonomic group throughout evolution. These patterns are relatively constant; however, both patterns and the magnitudes of integration may vary across species. These differences may indicate morphological diversification, in some cases related to functional adaptations to the biomechanics of organisms. In this study, we analyze patterns of integration between two functional and developmental structures, the cranium and the cervical spine in hominids, and we quantify the amount of divergence of each anatomical element through phylogeny. We applied these methods to three-dimensional data from 168 adult hominid individuals, summing a total of more than 1000 cervical vertebrae. We found the atlas (C1) and axis (C2) display the lowest covariation with the cranium in hominids (Homo sapiens, Pan troglodytes, Pan paniscus, Gorilla gorilla, Gorilla beringei, Pongo pygmaeus). H. sapiens show a relatively different pattern of craniocervical correlation compared with chimpanzees and gorillas, especially in variables implicated in maintaining the balance of the head. Finally, the atlas and axis show lower magnitude of shape change during evolution than the rest of the cervical vertebrae, especially those located in the middle of the subaxial cervical spine. Overall, results suggest that differences in the pattern of craniocervical correlation between humans and gorillas and chimpanzees could reflect the postural differences between these groups. Also, the stronger craniocervical integration and larger magnitude of shape change during evolution shown by the middle cervical vertebrae suggests that they have been selected to play an active role in maintaining head balance.
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The Weberian apparatus, a complex assemblage of greatly modified vertebral elements, significantly enhances hearing within Otophysi. Ultimately we are interested in investigating the genetic mechanisms responsible for the origin, development and morphological diversification of these vertebral elements in the Weberian apparatus of otophysan fishes. However, a necessary first step involves identifying changes in growth of this region as compared with the vertebrae from which these modified elements purportedly derive. Using an ontogenetic series of the zebrafish, Danio rerio, we collected growth data for specific elements within the Weberian apparatus, including neural arches, ribs, and parapophyses. These data are compared to both serially homologous structures in posterior thoracic vertebrae (which act as internal controls) and vertebral elements from the same axial levels in three other non-otophysan teleosts. Significant differences in growth rate were found among serially homologous structures, as well as at equivalent axial levels in different species. Uniform changes in growth rates (in which all structures derived from a specific somite were equally affected) were not found, suggesting precise targeting of morphological change to specific structures. The variation in growth of anterior vertebrae in and among species was greater than expected. This variation in growth rates created developmental patterns unique to each species. Such patterns of growth may help illuminate the specific heterochronic mechanisms required for the origin and subsequent morphological diversification of the Weberian apparatus. This morphological diversity is exemplified by the multitude of forms seen in the cypriniform Weberian apparatus. Understanding patterns of growth in discrete elements of the Weberian apparatus allows us to hypothesize as to the specific developmental changes, likely constituting differences in gene expression in pathways involved in bone and cartilage differentiation, responsible for this morphological diversity.
6 Hox Genes and the Global Patterning of the Somitic Mesoderm
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The nature of the information that distinguishes the behavior of somites at different axial levels (such as neck versus trunk) is understood with far less detail. This chapter reviews the data that relate to the translation of local information into global patterning of the somitic mesoderm derivatives. The types of morphological variation are reviewed that are seen among vertebrate taxa that result from evolutionary changes in global patterning in the mesoderm. The aspects of local, or primary patterning within individual somites are described that are apparently universal within vertebrates. The morphological fate of the somitic mesoderm is also reviewed that are determined by classic experiments on model systems that indicate which somites contribute to which adult structures. Finally, experimental and comparative studies are presented that have investigated molecular genetic factors that may control global patterning. These factors provide a means of understanding intrinsic proximal events in the evolution of animal form.
Craniofacial abnormalities induced by the ectopic expression of homeobox gene
1997, Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis
In this paper I have tried to bring together work that highlights the role of homeobox genes in generating craniofacial form. I review both normal and disrupted embryogenesis and ask whether mis-expression of the homeobox genes outside their normal domains could be contributing to congenital facial abnormalities arising from either genetic or teratogenic actions. Experimentally generated transgenic mice carrying loss- or gain-of-function mutations in homeobox genes, in combination with their normal expression patterns, have allowed us to compile and test models of embryonic specification based around a Hox/homeobox code. These models form the basis on which the functional questions are considered. There are four major sections covering different experimental approaches designed to ectopically induce homeobox genes in the head. Transgenic mice, where heterologous promoters drive a given Hox gene in the head, have shown that the more posteriorly expressed Hox genes tend to have a significant effect only on the skull bones of mesodermal origin whereas those normally expressed more anteriorly, in the hindbrain and branchial arches, can affect more anterior branchial arch and neural crest-derived structures. Manipulation experiments which can induce homeobox genes in small, localised regions of the facial precursors show clear and dramatic effects of this expression on facial development. Null mutations in predicted repressors of Hox gene expression, however, do not appear to give rise to substantial craniofacial abnormalities. Retinoic acid, on the other hand, is well known for its teratogenic actions and its ability to induce Hox gene expression. Evidence is now accumulating that at least some of its teratogenic actions may be mediated by its regulation of the Hox and other homeobox genes in the head.

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Regular articleIs There a Link Between Changes in the Vertebral “hoxcode” and the Shape of Vertebrae? A Quantitative Study of Shape Change in the Cervical Vertebral Column of Mice

Abstract

Regular article
Is There a Link Between Changes in the Vertebral “hoxcode” and the Shape of Vertebrae? A Quantitative Study of Shape Change in the Cervical Vertebral Column of Mice