Evolution of polarized hair cells in aquatic vertebrates and their connection to directionally sensitive neurons

Abstract

The mechanosensory hair cells enable aquatic vertebrates to maintain body position with respect to gravity, as well as to detect a wide variety of hydrodynamic (including hydroacoustic) stimuli. The evolution of hair-cell bearing sensory organs has been driven by the physical properties of the medium, which directs the adaptation of their molecular developmental program to extract information from different stimuli. Mutation and selection have shaped hair cell bearing organs to extract information about the distance, size, and movement direction to elicit motor behaviors, including avoidance, approach, or schooling in fish swarms. Here we will review some molecular, cellular, and developmental steps that outline a plausible evolution of hair cells and their use as hydrodynamic sensors in aquatic vertebrates. We suggest an evolutionary progression (from simple to complex) through multiplication of genes of the mechanosensory hair cell followed by cellular and organ diversification. We posit that this cell evolved, through morphological intermediates, which transformed the kinocilium surrounded by microvilli of the unicellular ancestor of metazoans into the polarized stereocilia of vertebrate hair cells. Anaxonic sensory cells of vertebrates have evolved, after an ancestral gene duplication, into both neurons and hair cells. Evolution of novel genes allowed the formation of discrete sensory organs such as the inner ear and the lateral line. An interesting but incompletely understood aspect of this evolution is the generation of hair-cell polarization and their distribution within sensory epithelia and their innervation.