Evolution of vertebrate mechanosensory hair cells and inner ears: toward identifying stimuli that select mutation driven altered morphologies

Abstract

Among the major distance senses of vertebrates, the ear is unique in its complex morphological changes during evolution. Conceivably, these changes enable the ear to adapt toward sensing various physically well-characterized stimuli. This review develops a scenario that integrates sensory cell with organ evolution. We propose that molecular and cellular evolution of the vertebrate hair cells occurred prior to the formation of the vertebrate ear. We previously proposed that the genes driving hair cell differentiation, were aggregated in the otic region through developmental re-patterning that generated a unique vertebrate embryonic structure, the otic placode. In agreement with the presence of graviceptive receptors in many vertebrate outgroups, it is likely that the vertebrate ear originally functioned as a simple gravity-sensing organ. Based on the rare occurrence of angular acceleration receptors in vertebrate outgroups, we further propose that the canal system evolved with a more sophisticated ear morphogenesis. This evolving morphogenesis obviously turned the initial otocyst into a complex set of canals and recesses, harboring multiple sensory epithelia each adapted to the acquisition of a specific aspect of a given physical stimulus. As support for this evolutionary progression, we provide several details of the molecular basis of ear development.

Connecting Ears to Eye Muscles: Evolution of a ‘Simple' Reflex Arc

“…Experimental evidence suggests that in vertebrates the respective gene products are essential for normal hair cell differentiation [Soukup et al, 2009;Pan et al, 2012]. Thus, the evolution of hair cells likely predates ear evolution, replacing previous hypotheses of ear evolution by a 'hair cell first' hypothesis [Duncan and Fritzsch, 2012;Fritzsch and Straka, 2014]. The 'hair cell first' hypothesis brings into focus the problem of the evolution of the dorsolateral placodes that give rise to ears and lateral line organs.…”

“…Whereas Pax6 is uniquely associated with eye development [Gehring, 2011], Pax2/5/8 is related to multiple organ systems such as kidney and ear [Bouchard et al, 2010;Christophorou et al, 2010]. While Pax genes are important for ear placode formation and development, additional transcription factors are also required [Chen and Streit, 2013;Fritzsch and Straka, 2014].…”

“…Importantly, none of the deuterostome outgroups of vertebrates have otoconiabearing sensory organs for gravity-dependent orientation, suggesting that the vertebrate otoconia-bearing ear is a novelty within the deuterostome lineage . However, many deuterostomes have at least cellular precursors that presage the morphological evolution of the vertebrate hair cells Burighel et al, 2011;Fritzsch and Straka, 2014]. These primordial and definitive hair cells can be identified not only by their morphological similarities but also by their expression of a unique set of transcription factors and microRNAs [Pierce et al, 2008;Candiani et al, 2011;Joyce Tang et al, 2013].…”

“…The transformation of a placode into a complex labyrinth with properly positioned, multiple sensory epithelia depends on many factors Chang et al, 2008;Fritzsch and Straka, 2014]. Lamprey and hagfish lack a lateral/horizontal canal and the expression of genes relevant for forming this canal.…”

Segregating neural and mechanosensory fates in the developing ear: patterning, signaling, and transcriptional control

“…Vertebrate hair cells are secondary receptor cells: they do not elaborate either axons or dendrites, but are innervated by axons of bipolar sensory neurons that also send processes to brainstem nuclei. Many non-vertebrate taxa possess mechanoreceptive cells with similar apical specializations; these are also sometimes referred to as hair cells, although their degree of homology to vertebrate hair cells is still actively debated (Burighel, et al, 2011, Burighel, et al, 2008, Burighel, et al, 2003, Fritzsch and Straka, 2014, Manley and Ladher, 2008). These non-vertebrate “hair cells” cells can be either secondary receptors, or primary sensory neurons with intrinsic mechanosensitive specializations (Burighel, et al, 2011).…”