Evolution of sound and balance perception: innovations that aggregate single hair cells into the ear and transform a gravistatic sensor into the organ of corti

Abstract

Here, we review the molecular basis of mechanosensory cell and mechanosensory organ development and evolution with an emphasis on the conservation of transcription factors and emerging data on conserved gene networks. The ear, the organ of vertebrates dedicated to the perception of sound and balance, perceives these stimuli with the use of mechanosensory cells. The developmental gene regulatory network used during mechanosensory cellular development has been conserved from ancient bilaterian cells, and modified for the extraction of specific mechanical stimuli resulting in phenotypic changes. In the vertebrate lineage, mechanosensory cells became specialized as gravistatic sensors after they became aggregated to form the ear. After this aggregation, growth, including duplication and segregation of existing neurosensory epithelia, gave rise to new epithelia and can be appreciated by comparing sensory epithelia from the inner ears of different vertebrates and their innervation by different neuronal populations. Novel directions of differentiation were apparently further expanded by incorporating unique molecular modules in newly developed sensory epithelia. For example, the saccule gave rise to the auditory epithelium and corresponding neuronal population of tetrapods, starting possibly in an aquatic environment. This novel sensory perception was followed by emergence of the central auditory nuclei and a selective cochlear nucleus projection. The data for this process is outlined and contrasted with other ideas dealing with a subset of the data.