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Extraocular vision in a brittle star is mediated by chromatophore movement in response to ambient light

Abstract:
Almost all animals can sense light, but only those with spatial vision can ‘see’. Conventionally this was restricted to animals possessing discrete visual organs (eyes), but extraocular vision could facilitate vision without eyes. Echinoderms form the focus of extraocular vision research [1–7], and the brittle star Ophiocoma wendtii, which exhibits light-responsive colour-change and shelter-seeking, became a key species of interest [4,8,9]. Both O. wendtii and an apparently light-indifferent congeneric, O. pumila, possess an extensive network of r-opsin-reactive cells, but its function remains unclear [4]. We show that although both species are strongly light-averse, O. wendtii orients to stimuli necessitating spatial vision for detection, but O. pumila does not. However, O. wendtii’s response disappears when chromatophores are contracted within the skeleton. Combining immunohistochemistry, histology and synchrotron microtomography, we reconstructed models of photoreceptors in situ and extracted estimated angular apertures for O. wendtii and O. pumila. Angular sensitivity estimates, derived from these models, support the hypothesis that chromatophores constitute a screening mechanism in O. wendtii, providing sufficient resolving power to detect the stimuli. RNA-Seq identified opsin candidates in both species, including multiple r-opsins and transduction pathway constituents, congruent with immunohistochemistry and studies of other echinoderms [10,11]. Finally, we note that differing body postures between the two species during experiments may reflect aspect of signal integration. This represents one of the most detailed mechanisms for extraocular vision yet proposed, and draws interesting parallels with the only other confirmed extraocular visual system, that of some sea urchins, which also possess chromatophores.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1016/j.cub.2019.11.042

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Institution:
University of Oxford
Department:
Natural History Museum
Oxford college:
St Anne's College
Role:
Author
ORCID:
0000-0003-0196-5069


Publisher:
Elsevier
Journal:
Current Biology More from this journal
Volume:
30
Issue:
2
Pages:
319-327.E4
Publication date:
2020-01-02
Acceptance date:
2019-11-13
DOI:
EISSN:
1879-0445
ISSN:
0960-9822


Language:
English
Pubs id:
pubs:1071809
UUID:
uuid:af5e50c0-661b-4c83-8557-387984ecaedb
Local pid:
pubs:1071809
Source identifiers:
1071809
Deposit date:
2019-11-14

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