Integration of the sensory and skeletal systems: A classical perspective on neuromast-bone interactions

The question of how morphological features of the vertebrate face evolve over deep geologic time can be inferred, in part, from the fossil record. However, paleontological evidence does not inform the developmental processes governing facial form and patterning. Insight to this fundamental feature of evolution, therefore, must come from empirical studies in extant model systems. An essential developmental feature of vertebrate facial skeleton evolution is the integration between sensation and bone. In the classic literature, a longstanding observation is that the positions of certain facial bone primary ossification centers (i.e., bone initiation sites) co-localize to the precise positions of sensory organs called canal neuromasts. These organs can be found in stereotypical positions along the head and flank of extant and extinct specimens. Some early researchers proposed that a developmental relationship couples these sensory organs to underlying bones (or bony structures). The evidence to support this relationship, however, was sparse and many remained skeptical - or outright disputed - the existence of such an integrated relationship. Several researchers instead argued that co-localization of neuromasts and bone were merely coincidental. Here, we review the classic literature, summarizing contrasting claims of several authors, stretching back to 1882. This revealed that speculation around an integrative sensory-skeletal relationship fell into three general categories: the presence of a developmental relationship between the structures, the absence of a relationship, or the existence of an indirect relationship between the structures. In summarizing the classic literature, we present further evidence in support of a developmental relationship illuminated by contemporary findings. We propose sensory-skeletal integration is a key developmental mechanism that could be modeled in paleontological research to further inform processes of cranial evolution over deep geological time.