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Mechanism of phototaxis in marine zooplankton
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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“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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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Metadata
- 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
- Venue
- Nature
- Published
- 2008-11
- Volume
- 456
- Issue
- 7220
- Pages
- 395-399
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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