Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

  1. Csaba Verasztó
  2. Martin Gühmann
  3. Huiyong Jia
  4. Vinoth Babu Veedin Rajan
  5. Luis A Bezares-Calderón
  6. Cristina Piñeiro-Lopez
  7. Nadine Randle
  8. Réza Shahidi
  9. Nico K Michiels
  10. Shozo Yokoyama
  11. Kristin Tessmar
  12. Gáspár Jékely  Is a corresponding author
  1. Max Planck Institute for Developmental Biology, Germany
  2. Emory University, United States
  3. University of Vienna, Austria

Abstract

Ciliary and rhabdomeric photoreceptor cells represent two main lines of photoreceptor-cell evolution in animals. The two cell types coexist in some animals, however how these cells functionally integrate is unknown. We used connectomics to map synaptic paths between ciliary and rhabdomeric photoreceptors in the planktonic larva of the annelid Platynereis and found that ciliary photoreceptors are presynaptic to the rhabdomeric circuit. The behaviors mediated by the ciliary and rhabdomeric cells also interact hierarchically. The ciliary photoreceptors are UV-sensitive and mediate downward swimming in non-directional UV light, a behavior absent in ciliary-opsin knockout larvae. UV avoidance overrides positive phototaxis mediated by the rhabdomeric eyes such that vertical swimming direction is determined by the ratio of blue/UV light. Since this ratio increases with depth, Platynereis larvae may use it as a depth gauge during vertical migration. Our results revealed a functional integration of ciliary and rhabdomeric photoreceptor cells in a zooplankton larva.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, 3 and 4 and Figure 2-figure supplement 2.

Article and author information

Author details

  1. Csaba Verasztó

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6295-7148
  2. Martin Gühmann

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4330-0754
  3. Huiyong Jia

    Department of Biology, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Vinoth Babu Veedin Rajan

    Max F Perutz Laboratories, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2430-7395
  5. Luis A Bezares-Calderón

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Cristina Piñeiro-Lopez

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Nadine Randle

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7817-4137
  8. Réza Shahidi

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Nico K Michiels

    Max F Perutz Laboratories, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  10. Shozo Yokoyama

    Department of Biology, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Kristin Tessmar

    Max F Perutz Laboratories, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  12. Gáspár Jékely

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    g.jekely@exeter.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8496-9836

Funding

Deutsche Forschungsgemeinschaft

  • Luis A Bezares-Calderón

National Institutes of Health

  • Vinoth Babu Veedin Rajan
  • Shozo Yokoyama

Max-Planck-Gesellschaft (Open-access funding)

  • Gáspár Jékely

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Piali Sengupta, Brandeis University, United States

Publication history

  1. Received: March 6, 2018
  2. Accepted: May 28, 2018
  3. Accepted Manuscript published: May 29, 2018 (version 1)
  4. Version of Record published: June 26, 2018 (version 2)

Copyright

© 2018, Verasztó et al.

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

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  1. Csaba Verasztó
  2. Martin Gühmann
  3. Huiyong Jia
  4. Vinoth Babu Veedin Rajan
  5. Luis A Bezares-Calderón
  6. Cristina Piñeiro-Lopez
  7. Nadine Randle
  8. Réza Shahidi
  9. Nico K Michiels
  10. Shozo Yokoyama
  11. Kristin Tessmar
  12. Gáspár Jékely
(2018)
Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton
eLife 7:e36440.
https://doi.org/10.7554/eLife.36440

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