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. Anat Rec, 295:1760Rec, 295: -1774Rec, 295: , 2012. V C 2012 Wiley Periodicals, Inc. Keywords: evolution; hair cell; mechanosensor; mechanosensory cell first hypothesis Animal body plans are the result of genomic mutations that augment specific developmental processes by modifying the spatial and temporal regulation of thousands of genes followed by selection of these modifications. Fossil and comparative anatomical data can raise significant questions about the progression of specific evolutionary changes but rarely provide enough material to generate a plausible theory. Most importantly, fossil data cannot provide answers to the underlying questions of genetic changes that drive differential development through altered cis-regulatory gene networks. It is only through comparative and functional analyses of developmental gene regulatory networks that one can directly discover genomic modifi-

Gene-expression analysis of hair cell regeneration in the zebrafish lateral line

“…The lateral line system senses water motion and initiates the appropriate behavioral response for capturing prey, avoiding predators, and schooling. The morphology and function of sensory hair cells are evolutionarily conserved from fish to mammals (32,33). Lateral line hair cells are located in the center of a mechanosensory organ known as the neuromast and are surrounded by inner support cells and an outer ring of mantle cells.…”

Diversity in Fish Auditory Systems: One of the Riddles of Sensory Biology

“…Only genetic studies could unravel how orientation groups form during ontogeny, leading to the different orientation patterns. Knowledge about underlying genetic processes of pattern formation is increasing (Duncan and Fritzsch, 2012;Sienknecht et al, 2014) and is likely to shed new light on the evolution of different orientation patterns in different lineages.…”

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

“…It should be noted that a series of transformations, from simple concentric arrangements of structures at the apex of a cell to asymmetric specializations of the apical surface, has been proposed for metazoans Brain Behav Evol 2014;83:150-161 DOI: 10.1159/000357752 152 [Fritzsch et al, 2007;Manley and Ladher, 2008] which are likely mediated by genes associated with hair cell development [Duncan and Fritzsch, 2012]: -class A bHLH genes, which regulate neuronal and hair cell differentiation, evolved only in metazoans [Pan et al, 2012]; -approximately 22-nucleotide-long microRNAs, which are essential for neurosensory development [Kersigo et al, 2011], evolved only in metazoans [Pierce et al, 2008] and are highly conserved [Philippe et al, 2011], and -Wnt signaling evolved only in diploblastic organisms [Fairclough et al, 2013]. With the recent finding that Wnt signaling is unique to diploblastic organisms, we explore the link between Wnt signaling and the different aspects of planar cell polarity (PCP).…”

“…Ectopic hair cells of vestibular character develop in the nonsensory 'homogene cell' domain in chickens after forced activation of Wnt signaling [Stevens et al, 2003], indicating the maintained competence of this cochlear duct domain to generate hair cells. Several mouse mutants possess sensory epithelia that remain fused and display intermediate PCP patterns [Duncan and Fritzsch, 2012].…”