1. Developmental Biology
  2. Neuroscience
Download icon

Embryonic Development: The evolution of hearing and balance

  1. Forrest P Weghorst
  2. Karina S Cramer  Is a corresponding author
  1. University of California, Irvine, United States
Insight
  • Cited 0
  • Views 1,204
  • Annotations
Cite this article as: eLife 2019;8:e44567 doi: 10.7554/eLife.44567

Abstract

New genetic tools have allowed researchers to compare how the brainstem auditory and vestibular nuclei develop in embryonic chicks and mice.

Main text

The ear is an organ with two main roles – hearing and balance – and it relies on mechanically sensitive hair cells to perform both jobs. When the ear detects a sound, it sends signals to clusters of neurons called the brainstem auditory nuclei, and when it registers movement of the head, it sends signals to the brainstem vestibular nuclei. The vestibular nuclei are remarkably similar among vertebrates, from fish to humans (Fritzsch et al., 2014). However, the auditory nuclei display considerable diversity across species. For example, birds and mammals both have a pathway that uses the difference in the time of arrival of a sound at each ear to determine where the noise came from. However, this circuit works differently in these two groups of animals, suggesting that it may have emerged independently multiple times during evolution (Grothe and Pecka, 2014). How, then, did the modern auditory and vestibular nuclei arise?

One strategy to address this question is to explore the embryonic development of vertebrates. Nuclei in the brainstem arise from the embryonic hindbrain, which is remarkably similar across vertebrate species and is divided into segments called rhombomeres (Di Bonito and Studer, 2017). Fate mapping studies have been used to test whether cells in the auditory and vestibular nuclei of different vertebrate species derive from the same rhombomeres.

In this technique, embryonic tissue can be labeled with an external marker, such as a dye (for traditional fate mapping), or a fluorescent protein marker (for genetic fate mapping), in order to track the destination of the cells arising from that tissue (Stern and Fraser, 2001; Legué and Joyner, 2010). Previously, traditional fate mapping has been limited to research in birds (which have accessible embryos), while genetic fate mapping has been limited to mammals (which have accessible genomes; Cramer et al., 2000; Marín and Puelles, 1995; Kim and Dymecki, 2009).

However, both approaches have technical caveats and they identify progenitors in different ways, which hinders their direct comparison. Traditional fate mapping identifies the fate of all labeled cells within a restricted area of the embryo, which may contain a range of progenitor cell types. In contrast, genetic fate mapping marks only cells that express a certain gene (or genes), but these cells can come from a wider area within the embryo.

Now, in eLife, Marcela Lipovsek and Richard Wingate of King’s College London report how they have addressed this dilemma by using vector-based genetic fate mapping in chick embryos (Lipovsek and Wingate, 2018). The researchers focused on genes that were only active in certain regions of the embryonic hindbrain. Plasmid vectors were used to label cells with a fluorescent protein after specific genes in those cells were active. This way, the fate of cells along two anatomical axes (from head to tail, and from back to belly) could be traced. Lipovsek and Wingate studied the same genes that were previously used to construct genetic fate maps of brainstem nuclei in mice, which enabled them to draw direct comparisons between birds and mammals for the first time (Di Bonito and Studer, 2017).

Their results confirmed that vestibular nuclei have similar embryonic origins in chicks and mice. In contrast, auditory nuclei that have comparable roles in chicks and mice arise from completely different embryonic tissues. This suggests that birds and mammals used different populations of ancestral cells – often from different rhombomeres – to independently evolve circuits for calculating sound location.

Lipovsek and Wingate provide compelling evidence that the anatomical similarities between vestibular nuclei in birds and mammals are due to common developmental and evolutionary origins. And since their vestibular systems are also homologous to those of fish, it seems that the role of the vestibular organ remained relatively unaffected by our aquatic ancestors’ move to land (Fritzsch et al., 2014). Conversely, the different developmental origins of auditory nuclei in birds and mammals reflect how each clade solved the problem of hearing on land by adapting to its own ecological niche (Carr and Christensen-Dalsgaard, 2016).

References

  1. Book
    1. Fritzsch B
    2. Kopecky BJ
    3. Duncan JS
    (2014) Development of the mammalian ‘vestibular’ system: evolution of form to detect angular and gravity acceleration
    In: Romand R, Varela-Nieto I, editors. Development of Auditory and Vestibular Systems. San Diego: Academic Press. pp. 339–367.
    https://doi.org/10.1016/B978-0-12-408088-1.00012-9

Article and author information

Author details

  1. Forrest P Weghorst

    Forrest P Weghorst is in the Department of Neurobiology and Behavior, University of California, Irvine, United States

    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9365-1846
  2. Karina S Cramer

    Karina S Cramer is in the Department of Neurobiology and Behavior, University of California, Irvine, United States

    For correspondence
    cramerk@uci.edu
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3793-4862

Publication history

  1. Version of Record published: February 8, 2019 (version 1)

Copyright

© 2019, Weghorst and Cramer

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,204
    Page views
  • 136
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Developmental Biology
    Zhaoyang Liu et al.
    Research Article

    Adolescent idiopathic scoliosis (AIS) is the most common spine disorder affecting children worldwide, yet little is known about the pathogenesis of this disorder. Here, we demonstrate that genetic regulation of structural components of the axial skeleton, the intervertebral discs, and dense connective tissues (i.e., ligaments and tendons) are essential for the maintenance of spinal alignment. We show that the adhesion G protein-coupled receptor ADGRG6, previously implicated in human AIS association studies, is required in these tissues to maintain typical spine alignment in mice. Furthermore, we show that ADGRG6 regulates biomechanical properties of tendon and stimulates CREB signaling governing gene expression in cartilaginous tissues of the spine. Treatment with a cAMP agonist could mirror aspects of receptor function in culture, thus defining core pathways for regulating these axial cartilaginous and connective tissues. As ADGRG6 is a key gene involved in human AIS, these findings open up novel therapeutic opportunities for human scoliosis.

    1. Developmental Biology
    2. Genetics and Genomics
    Yukiko Tando et al.
    Research Article

    Exposure to environmental factors during fetal development may lead to epigenomic modifications in fetal germ cells, altering gene expression and promoting diseases in successive generations. In mouse, maternal exposure to di(2-ethylhexyl) phthalate (DEHP) is known to induce defects in spermatogenesis in successive generations, but the mechanism(s) of impaired spermatogenesis are unclear. Here, we showed that maternal DEHP exposure results in DNA hypermethylation of promoters of spermatogenesis-related genes in fetal testicular germ cells in F1 mice, and hypermethylation of Hist1h2ba, Sycp1, and Taf7l, which are crucial for spermatogenesis, persisted from fetal testicular cells to adult spermatogonia, resulting in the downregulation of expression of these genes. Forced methylation of these gene promoters silenced expression of these loci in a reporter assay. These results suggested that maternal DEHP exposure-induced hypermethylation of Hist1h2ba, Sycp1, and Taf7l results in downregulation of these genes in spermatogonia and subsequent defects in spermatogenesis, at least in the F1 generation.