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Evolution of development of the vertebrate dermal and oral skeletons: unraveling concepts, regulatory theories, and homologies

Published online by Cambridge University Press:  08 April 2016

Philip C. J. Donoghue*
Affiliation:
Lapworth Museum of Geology, School of Geography, Earth and Environmental Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom. E-mail: [email protected]

Abstract

It has been contended that Reif's odontode regulation theory is a rival and alternative to Stensiö and ørvig's lepidomorial theory as means of explaining the evolution of development of the vertebrate dermal and oral skeleton. The lepidomorial theory is a pattern-based theory that provides a homological framework that goes further than the odontode regulation theory in comparing dental papillae and their products, and it provides an explanatory mechanism for such relationships a posteriori. In contrast, the odontode regulation theory is process-based and observes only developmental similarity, providing no means of identifying homologies beyond this. The lepidomorial theory is superior to the odontode regulation theory in its ability to trace homology through the evolution of development of the dermal and oral skeleton. The criteria proposed to identify homology between scales—either within a given individual or taxon, or between different individuals or taxa—are, primarily, vascular architecture and, secondarily, external morphology. External morphology may be excluded on Reif's argument for the overarching principle of differentiation, a hypothesis supported by recent advances in the understanding of dental morphogenesis. Vascular architecture is potentially useful but appears to be determined by tooth/scale morphology rather than reflecting historical (phylogenetic) constraint. Data on the development of epithelial appendages, including teeth, scales, and feathers, indicate that individual primordia develop through progressive differentiation of originally larger, homogenous morphogenetic fields. Thus, there is no mechanism of ontogenetic developmental concrescence, just differentiation. Phylogenetic patterns of concrescence and differentiation are similarly achieved through ontogenetic developmental differentiation, or a lack thereof. In practice, however, it is not possible to distinguish between patterns of phylogenetic concrescence and differentiation because there is no means of identifying homology between individual elements within a squamation, or a dentition (in almost all instances). Thus, phylogenetic patterns of increase and decrease in the numbers of elements constituting dentitions or dermal elements are best described as such; further attempts to constrain precise underlying patterns remain without constraint and outside the realms of scientific enquiry. The application of the homology concept in the dermal and visceral skeletons is explored and it is determined that odontodes are serial homologs, conform only to the biological homology concept at this level of observation, and are devoid of phylogenetic meaning. It is concluded that Reif's theory is close to a universal theory of the evolution of development for the dermoskeleton and dentition, and additional components of theory, including the regulatory basis of temporal and spatial patterning, are tested and extended in light of data on the development of the chick feather array. Finally, the dermoskeleton is identified as an exemplary system for examining the regulatory basis of patterning and morphogenesis as it encompasses and surpasses the repertoire of established model organ systems.

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Articles
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Copyright © The Paleontological Society 

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References

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