Evolution and development of the tetrapod auditory system: an organ of Corti‐centric perspective

Abstract

The tetrapod auditory system transmits sound through the outer and middle ear to the organ of Corti or other sound pressure receivers of the inner ear where specialized hair cells translate vibrations of the basilar membrane into electrical potential changes that are conducted by the spiral ganglion neurons to the auditory nuclei. In other systems, notably the vertebrate limb, a detailed connection between the evolutionary variations in adaptive morphology and the underlying alterations in the genetic basis of development has been partially elucidated. In this review, we attempt to correlate evolutionary and partially characterized molecular data into a cohesive perspective of the evolution of the mammalian organ of Corti out of the tetrapod basilar papilla. We propose a stepwise, molecularly partially characterized transformation of the ancestral, vestibular developmental program of the vertebrate ear. This review provides a framework to decipher both discrete steps in development and the evolution of unique functional adaptations of the auditory system. The combined analysis of evolution and development establishes a powerful cross-correlation where conclusions derived from either approach become more meaningful in a larger context not possible through exclusively evolution or development centered perspectives.

Development of oculomotor circuitry independent of hox3 genes

“…The previously mentioned auditory circuits in mice exhibited connections with the cochlea, a mammalian-only end-organ 63 . The observed Hox dependence 63 could represent an evolutionary transformation correlating with increased circuit complexity.…”

“…The previously mentioned auditory circuits in mice exhibited connections with the cochlea, a mammalian-only end-organ 63 . The observed Hox dependence 63 could represent an evolutionary transformation correlating with increased circuit complexity. By contrast, the horizontal and torsional/vertical vestibuloocular and optokinetic circuitry in fish have a lengthy evolutionary history, traceable to agnatha (jawless fish) 64-66 .…”

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

“…We will not discuss scenarios for the development of the mammalian ear and auditory pathways. For recent reviews of mammalian ear evolution, the reader is directed to Manley [2012, 2016] and Fritzsch and Straka [2014], and for discussions of mammalian auditory pathways, see Grothe et al [2005], Fritzsch et al [2013], and Nothwang [2016].…”

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

“…Other factors, such as homeobox genes Fgf s and BMP s [Chang et al, 2008], also play a role in this process, and the inner ear shows dramatic malformations or incomplete segregation of sensory epithelia in many mutants, such as the Lmx1a null mutation [Nichols et al, 2008]. The emerging picture implies a progressive transformation of a simple ear, as found in jawless vertebrates, through formation of multiple recesses, each associated with its own sensory epithelium, into the complex labyrinth of jawed vertebrates [Fritzsch et al, 2013] paralleled by a concurrent segregation of sensory afferent innervation [de Burlet, 1934;Fritzsch et al, 2002].…”