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Research Article
The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina
Fanny de Busserolles, Fabio Cortesi, Lily Fogg, Sara M. Stieb, Martin Luehrmann, N. Justin Marshall
Journal of Experimental Biology 2021 224: jeb233098 doi: 10.1242/jeb.233098 Published 13 January 2021
Fanny de Busserolles
1Queensland Brain Institute, The University of Queensland, Brisbane, QLD 4072, Australia
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  • ORCID record for Fanny de Busserolles
  • For correspondence: f.debusserolles@uq.edu.au
Fabio Cortesi
1Queensland Brain Institute, The University of Queensland, Brisbane, QLD 4072, Australia
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Lily Fogg
1Queensland Brain Institute, The University of Queensland, Brisbane, QLD 4072, Australia
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Sara M. Stieb
1Queensland Brain Institute, The University of Queensland, Brisbane, QLD 4072, Australia
2Center for Ecology, Evolution and Biogeochemistry, Eawag Federal Institute of Aquatic Science and Technology, Seestrasse 79, 6074 Kastanienbaum, Switzerland; and Institute for Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012 Bern, Switzerland
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Martin Luehrmann
1Queensland Brain Institute, The University of Queensland, Brisbane, QLD 4072, Australia
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N. Justin Marshall
1Queensland Brain Institute, The University of Queensland, Brisbane, QLD 4072, Australia
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ABSTRACT

The visual systems of teleost fishes usually match their habitats and lifestyles. Since coral reefs are bright and colourful environments, the visual systems of their diurnal inhabitants have been more extensively studied than those of nocturnal species. In order to fill this knowledge gap, we conducted a detailed investigation of the visual system of the nocturnal reef fish family Holocentridae. Results showed that the visual system of holocentrids is well adapted to their nocturnal lifestyle with a rod-dominated retina. Surprisingly, rods in all species were arranged into 6–17 well-defined banks, a feature most commonly found in deep-sea fishes, that may increase the light sensitivity of the eye and/or allow colour discrimination in dim light. Holocentrids also have the potential for dichromatic colour vision during the day with the presence of at least two spectrally different cone types: single cones expressing the blue-sensitive SWS2A gene, and double cones expressing one or two green-sensitive RH2 genes. Some differences were observed between the two subfamilies, with Holocentrinae (squirrelfish) having a slightly more developed photopic visual system than Myripristinae (soldierfish). Moreover, retinal topography of both ganglion cells and cone photoreceptors showed specific patterns for each cell type, likely highlighting different visual demands at different times of the day, such as feeding. Overall, their well-developed scotopic visual systems and the ease of catching and maintaining holocentrids in aquaria, make them ideal models to investigate teleost dim-light vision and more particularly shed light on the function of the multibank retina and its potential for dim-light colour vision.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: F.d.B., F.C., S.M.S., N.J.M.; Methodology: F.d.B., F.C., S.M.S., M.L.; Validation: F.d.B., F.C., S.M.S.; Formal analysis: F.d.B., F.C., S.M.S., L.F., M.L.; Investigation: F.d.B., F.C., L.F., S.M.S.; M.L., Resources: F.d.B., F.C., S.M.S., N.J.M.; Writing - original draft: F.d.B.; Writing - review & editing: F.d.B., F.C., L.F., S.M.S., M.L., N.J.M.; Visualization: F.d.B., F.C., L.F., S.M.S.; Supervision: F.d.B., N.J.M.; Project administration: F.d.B.; Funding acquisition: F.d.B., N.J.M.

  • Funding

    This research was supported by several Australian Research Council (ARC) grants, an ARC Laureate Fellowship (FL140100197) awarded to N.J.M. and ARC DECRA awarded to F.d.B. (DE180100949) and F.C. (DE200100620). In addition, F.C. was also supported by a University of Queensland Development Fellowship and a Swiss National Science Foundation Early Postdoc Mobility Fellowship and S.M.S. was supported by the German Research Foundation (DFG).

  • Data availability

    Raw-read transcriptomes (PRJNA674704, SAMN16670685–SAMN16670689) and single gene sequences (MW219662-MW219691) are available through GenBank (https://www.ncbi.nlm.nih.gov/genbank/). Gene alignments, phylogenies, transcriptome assemblies, sensitivity prediction alignments and additional tables and figures are available from the Dryad digital repository (de Busserolles et al., 2021): nvx0k6dr3.

  • Supplementary information

    Supplementary information available online at https://jeb.biologists.org/lookup/doi/10.1242/jeb.233098.supplemental

  • Received July 23, 2020.
  • Accepted November 16, 2020.
  • © 2021. Published by The Company of Biologists Ltd
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Keywords

  • Colour vision
  • Dim-light vision
  • Holocentrid
  • Multibank retina
  • Teleost fish
  • Nocturnal coral reef fish

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Research Article
The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina
Fanny de Busserolles, Fabio Cortesi, Lily Fogg, Sara M. Stieb, Martin Luehrmann, N. Justin Marshall
Journal of Experimental Biology 2021 224: jeb233098 doi: 10.1242/jeb.233098 Published 13 January 2021
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Research Article
The visual ecology of Holocentridae, a nocturnal coral reef fish family with a deep-sea-like multibank retina
Fanny de Busserolles, Fabio Cortesi, Lily Fogg, Sara M. Stieb, Martin Luehrmann, N. Justin Marshall
Journal of Experimental Biology 2021 224: jeb233098 doi: 10.1242/jeb.233098 Published 13 January 2021

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