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 1,134
  • 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. 1
  2. 2
  3. 3
  4. 4
    Development of the mammalian ‘vestibular’ system: evolution of form to detect angular and gravity acceleration
    1. B Fritzsch
    2. BJ Kopecky
    3. JS Duncan
    (2014)
    In: R Romand, I Varela-Nieto, 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
  5. 5
  6. 6
  7. 7
  8. 8
  9. 9
  10. 10

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

  • 1,134
    Page views
  • 126
    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
    Feng Wang et al.
    Research Article

    The X-linked gene Rlim plays major roles in female mouse development and reproduction, where it is crucial for the maintenance of imprinted X chromosome inactivation in extraembryonic tissues of embryos. However, while females carrying a systemic Rlim knockout (KO) die around implantation, male Rlim KO mice appear healthy and are fertile. Here we report an important role for Rlim in testis where it is highly expressed in post-meiotic round spermatids as well as in Sertoli cells. Systemic deletion of the Rlim gene results in lower numbers of mature sperm that contains excess cytoplasm, leading to decreased sperm motility and in vitro fertilization rates. Targeting the conditional Rlim cKO specifically to the spermatogenic cell lineage largely recapitulates this phenotype. These results reveal functions of Rlim in male reproduction specifically in round spermatids during spermiogenesis.

    1. Cell Biology
    2. Developmental Biology
    Radek Jankele et al.
    Research Article

    Asymmetric divisions that yield daughter cells of different sizes are frequent during early embryogenesis, but the importance of such a physical difference for successful development remains poorly understood. Here, we investigated this question using the first division of C. elegans embryos, which yields a large AB cell and a small P1 cell. We equalized AB and P1 sizes using acute genetic inactivation or optogenetic manipulation of the spindle positioning protein LIN-5. We uncovered that only some embryos tolerated equalization, and that there was a size asymmetry threshold for viability. Cell lineage analysis of equalized embryos revealed an array of defects, including faster cell cycle progression in P1 descendants, as well as defects in cell positioning, division orientation and cell fate. Moreover, equalized embryos were more susceptible to external compression. Overall, we conclude that unequal first cleavage is essential for invariably successful embryonic development of C. elegans.