Molecular evolution of the vertebrate mechanosensory cell and ear

Abstract

The molecular basis of mechanosensation, mechanosensory cell development and mechanosensory organ development is reviewed with an emphasis on its evolution. In contrast to eye evolution and development, which apparently modified a genetic program through intercalation of genes between the master control genes on the top (Pax6, Eya1, Six1) of the hierarchy and the structural genes (rhodopsin) at the bottom, the as yet molecularly unknown mechanosensory channel precludes such a firm conclusion for mechanosensors. However, recent years have seen the identification of several structural genes which are involved in mechanosensory tethering and several transcription factors controlling mechanosensory cell and organ development; these warrant the interpretation of available data in very much the same fashion as for eye evolution: molecular homology combined with potential morphological parallelism. This assertion of molecular homology is strongly supported by recent findings of a highly conserved set of microRNAs that appear to be associated with mechanosensory cell development across phyla. The conservation of transcription factors and their regulators fits very well to the known or presumed mechanosensory specializations which can be mostly grouped as variations of a common cellular theme. Given the widespread distribution of the molecular ability to form mechanosensory cells, it comes as no surprise that structurally different mechanosensory organs evolved in different phyla, presenting a variation of a common theme specified by a conserved set of transcription factors in their cellular development. Within vertebrates and arthropods, some mechanosensory organs evolved into auditory organs, greatly increasing sensitivity to sound through modifications of accessory structures to direct sound to the specific sensory epithelia. However, while great attention has been paid to the evolution of these accessory structures in vertebrate fossils, comparatively less attention has been spent on the evolution of the inner ear and the central auditory system. Recent advances in our molecular understanding of ear and brain development provide novel avenues to this neglected aspect of auditory neurosensoy evolution.

Conserved gene regulatory module specifies lateral neural borders across bilaterians

“…Hence, more molecular and comparative studies are needed to understand the evolutionary relationship of these mechanosensing cell types. Nevertheless, our study on the neural borders suggests the conservation of the molecular mechanism underlying the specification of PNS progenitors across bilaterians (39).…”

Transplantation of Xenopus laevis ears reveals the ability to form afferent and efferent connections with the spinal cord

“…Combined these data could be interpreted to imply that in vertebrates, the ear develops in place of a somite or somitomere. If true, the facial branchial motor neurons destined to innervate the somiteor somitomere-derived muscle fibers may have been rerouted to innervate the ear when the ear evolved in ancestral vertebrates (Fritzsch et al, 2007).…”

Familiar Meniere's disease restricted to 1.48 Mb on chromosome 12p12.3 by allelic and haplotype association

“…Recent studies in mice and humans have established the importance of microRNAs (miRNAs) in the development and function of the inner ear. [36][37][38][39][40][41][42][43][44][45][46] Point mutations in the seed region of miR-96, an miRNA expressed in hair cells of the inner ear, result in autosomal dominant, progressive hearing loss. 43,47 Mice mutant for several of the target genes for miRNAs exhibit deafness and hair cell degeneration, indicating the importance of this novel gene regulation in hearing loss.…”