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Cited by 298Marine Invertebrate Physiology and EcologyVisual perception and processing mechanismsNeurobiology and Insect Physiology Research

Mechanism of phototaxis in marine zooplankton

Jékely, Gáspár, Colombelli, Julien, Hausen, Harald, Guy, Keren, Stelzer, Ernst, Nédélec, François, Arendt, Detlev·2008·Nature
DOI 10.1038/nature07590
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Abstract

The simplest animal eyes are eyespots composed of two cells only: a photoreceptor and a shading pigment cell. They resemble Darwin's 'proto-eyes', considered to be the first eyes to appear in animal evolution. Eyespots cannot form images but enable the animal to sense the direction of light. They are characteristic for the zooplankton larvae of marine invertebrates and are thought to mediate larval swimming towards the light. Phototaxis of invertebrate larvae contributes to the vertical migration of marine plankton, which is thought to represent the biggest biomass transport on Earth. Yet, despite its ecological and evolutionary importance, the mechanism by which eyespots regulate phototaxis is poorly understood. Here we show how simple eyespots in marine zooplankton mediate phototactic swimming, using the marine annelid Platynereis dumerilii as a model. We find that the selective illumination of one eyespot changes the beating of adjacent cilia by direct cholinergic innervation resulting in locally reduced water flow. Computer simulations of larval swimming show that these local effects are sufficient to direct the helical swimming trajectories towards the light. The computer model also shows that axial rotation of the larval body is essential for phototaxis and that helical swimming increases the precision of navigation. These results provide, to our knowledge, the first mechanistic understanding of phototaxis in a marine zooplankton larva and show how simple eyespots regulate it. We propose that the underlying direct coupling of light sensing and ciliary locomotor control was a principal feature of the proto-eye and an important landmark in the evolution of animal eyes.

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Crossref · 10.1038/nature07590

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33 of 33 references verified0 citation errors · 0 not checkable

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  • Ciliary bands can be controlled directly by multifunctional sensory-motor cells, as during phototaxis in Platynereis dumerilii larvae.

    “Ciliary bands can be controlled directly by multifunctional sensory-motor cells, as during phototaxis in the larvae of the annelid Platynereis dumerilii (figure 2) [25].”

    From An option space for early neural evolution (2015) · cites this paper as [25]

  • The single-celled Chlamydomonas, the multicellular Volvox or the larvae of the annelid Platynereis all orient very quickly and precisely along the light vector, usually within a few helical turns.

    “The single-celled Chlamydomonas [26], the multicellular Volvox [35] or the larvae of the annelid Platynereis [8] all orient very quickly and precisely along the light vector, usually within a few helical turns.”

    From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [8]

  • The sensory-motor phototactic eyes, directly synapsing on ciliated cells in the larvae of the annelid Platynereis, represent an ancestral stage in eye circuit evolution.

    “We argued recently that the sensory-motor phototactic eyes, directly synapsing on ciliated cells in the larvae of the annelid Platynereis represent such an ancestral stage in eye circuit evolution [8].”

    From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [8]

  • From a circuit evolution perspective, the concentration of ciliary motors into a few cells allows a very significant saving on wire length, cell number and synapse number.

    “However, from a circuit evolution perspective, the concentration of ciliary motors into a few cells (e.g. two rows of 12 multiciliated cells in the annelid Platynereis; [8]) allows a very significant saving on wire length, cell number and synapse number.”

    From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [8]

  • Our results support the view that the larval eyes and brain of annelids, and probably other spiralians, represent more closely an ancestral stage of brain evolution.

    “Even though the evolutionary origin and ancient versus modern origin of larvae is still debated [73,74], our results support the view that the larval eyes and brain of annelids (and probably other spiralian) represent more closely an ancestral stage of brain evolution [8].”

    From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [8]

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Authors
Jékely, G., Colombelli, J., Hausen, H., Guy, K., Stelzer, E., Nédélec, F., & Arendt, D.
Affiliations
  • Max Planck Institute for Developmental Biology (DE)
  • European Molecular Biology Laboratory (DE)
  • Freie Universität Berlin (DE)
Corresponding author
  • Jékely, Gáspár
  • Arendt, Detlev
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2008-11
Volume
456
Issue
7220
Pages
395-399
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/nature07590
OpenAlex
W2035277980
Cited by
298
References
33
Citations by year
2026: 12 · 2025: 29 · 2024: 13 · 2023: 15 · 2022: 13 · 2021: 19 · 2020: 28 · 2019: 18 · 2018: 18 · 2017: 25 · 2016: 17 · 2015: 19 · 2014: 22 · 2013: 13 · 2012: 8
FWCI
7.39
Type
journal article
Language
en
Open access
closed
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords
phototaxis, eyespots, Platynereis dumerilii, ciliary beating, cholinergic innervation, helical swimming, vertical migration, optical sensing, axial rotation
MeSH terms
Animals, Annelida, Cilia, Computer Simulation, Eye, Larva, Light, Locomotion, Receptors, Nicotinic, Swimming, Vision, Ocular, Zooplankton, Photoreceptor Cells, Invertebrate

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