Conserved and divergent development of brainstem vestibular and auditory nuclei.

Marcela Lipovsek,Richard JT Wingate

doi:10.7554/elife.40232

Abstract

Vestibular function was established early in vertebrates and has remained, for the most part, unchanged. In contrast, each group of tetrapods underwent independent evolutionary processes to solve the problem of hearing on land, resulting in a remarkable mixture of conserved, divergent and convergent features that define extant auditory systems. The vestibuloacoustic nuclei of the hindbrain develop from a highly conserved ground plan and provide an ideal framework on which to address the participation of developmental processes to the evolution of neuronal circuits. We employed an electroporation strategy to unravel the contribution of two dorsoventral and four axial lineages to the development of the chick hindbrain vestibular and auditory nuclei. We compare the chick developmental map with recently established genetic fate-maps of the developing mouse hindbrain. Overall, we find considerable conservation of developmental origin for the vestibular nuclei. In contrast, a comparative analysis of the developmental origin of hindbrain auditory structures echoes the complex evolutionary history of the auditory system. In particular, we find that the developmental origin of the chick auditory interaural time difference circuit supports its emergence from an ancient vestibular network, unrelated to the analogous mammalian counterpart.

Highlights

The colonisation of land by tetrapods led to a series of independent solutions to the problem of adapting sensory systems from water to air
In order to determine the developmental origin of hindbrain auditory and vestibular nuclei, we performed in ovo electroporation of chick embryos at stages 12 to 14 (Figure 2A) with two contrasting sets of conditional reporter constructs
We evaluate the contribution of changes in hindbrain development to the evolution of neuronal circuits, within the context of disparaging evolutionary histories of the different amniote vestibular and auditory structures

Summary

Introduction

The colonisation of land by tetrapods led to a series of independent solutions to the problem of adapting sensory systems from water to air. Most striking amongst them is the independent emergence during the Triassic period, more than 100 million years after the separation of the tetrapod lineages, of at least five variants of a tympanic middle ear, which operates as an impedance matching device for the efficient detection of airborne sounds (Anthwal et al, 2013; Carr and Christensen-Dalsgaard, 2016; Clack, 2015; Kitazawa et al, 2015; Manley, 2000; Tucker, 2017) This was accompanied by the independent elongation of the auditory sensory epithelia, a parallel diversification of hair cell types and concomitant elaborations of hair cell based sound amplification mechanisms, leading to fine tuning of sound detection and expansions of the hearing range to higher frequencies in several amniote clades (Dallos, 2008; Hudspeth, 2008; Koppl, 2011; Manley, 2000; Manley, 2017). Functionally analogous circuit components in the ITD circuit of the chick and mouse have different lineage contributions supporting a long-held hypothesis that they represent an example of evolutionary convergence

Results

Discussion

Materials and methods

Funding Funder Royal Society