Pushing the limits of photoreception in twilight conditions: The rod-like cone retina of the deep-sea pearlsides

Handle URI:
http://hdl.handle.net/10754/626202
Title:
Pushing the limits of photoreception in twilight conditions: The rod-like cone retina of the deep-sea pearlsides
Authors:
Busserolles, Fanny de ( 0000-0002-4602-9840 ) ; Cortesi, Fabio ( 0000-0002-7518-6159 ) ; Helvik, Jon Vidar; Davies, Wayne I. L.; Templin, Rachel M. ( 0000-0003-2800-5826 ) ; Sullivan, Robert K. P. ( 0000-0003-3414-2448 ) ; Michell, Craig T.; Mountford, Jessica K. ( 0000-0002-3293-6327 ) ; Collin, Shaun P. ( 0000-0001-6236-0771 ) ; Irigoien, Xabier; Kaartvedt, Stein; Marshall, Justin ( 0000-0001-9006-6713 )
Abstract:
Most vertebrates have a duplex retina comprising two photoreceptor types, rods for dim-light (scotopic) vision and cones for bright-light (photopic) and color vision. However, deep-sea fishes are only active in dim-light conditions; hence, most species have lost their cones in favor of a simplex retina composed exclusively of rods. Although the pearlsides, Maurolicus spp., have such a pure rod retina, their behavior is at odds with this simplex visual system. Contrary to other deep-sea fishes, pearlsides are mostly active during dusk and dawn close to the surface, where light levels are intermediate (twilight or mesopic) and require the use of both rod and cone photoreceptors. This study elucidates this paradox by demonstrating that the pearlside retina does not have rod photoreceptors only; instead, it is composed almost exclusively of transmuted cone photoreceptors. These transmuted cells combine the morphological characteristics of a rod photoreceptor with a cone opsin and a cone phototransduction cascade to form a unique photoreceptor type, a rod-like cone, specifically tuned to the light conditions of the pearlsides' habitat (blue-shifted light at mesopic intensities). Combining properties of both rods and cones into a single cell type, instead of using two photoreceptor types that do not function at their full potential under mesopic conditions, is likely to be the most efficient and economical solution to optimize visual performance. These results challenge the standing paradigm of the function and evolution of the vertebrate duplex retina and emphasize the need for a more comprehensive evaluation of visual systems in general.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Red Sea Research Center (RSRC)
Citation:
De Busserolles F, Cortesi F, Helvik JV, Davies WIL, Templin RM, et al. (2017) Pushing the limits of photoreception in twilight conditions: The rod-like cone retina of the deep-sea pearlsides. Science Advances 3: eaao4709. Available: http://dx.doi.org/10.1126/sciadv.aao4709.
Publisher:
American Association for the Advancement of Science (AAAS)
Journal:
Science Advances
Issue Date:
9-Nov-2017
DOI:
10.1126/sciadv.aao4709
Type:
Article
ISSN:
2375-2548
Sponsors:
This work was supported by King Abdullah University of Science and Technology, the Air Force Office of Scientific Research, and the Australian Research Council via grants awarded to J.M.; a Discovery Project grant (DP140102117) and Future Fellowship (FT110100176) awarded to W.I.L.D.; and a Linkage Infrastructure, Equipment and Facilities (LIEF) grant (LE100100074) awarded to the Queensland Brain Institute (Neurolucida software). F.C. was supported by a Swiss National Science Foundation Early Postdoctoral Mobility Fellowship (165364) and a University of Queensland Development Fellowship. J.V.H. was supported by a start-up grant from the University of Bergen.
Additional Links:
http://advances.sciencemag.org/content/3/11/eaao4709
Appears in Collections:
Articles; Red Sea Research Center (RSRC); Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorBusserolles, Fanny deen
dc.contributor.authorCortesi, Fabioen
dc.contributor.authorHelvik, Jon Vidaren
dc.contributor.authorDavies, Wayne I. L.en
dc.contributor.authorTemplin, Rachel M.en
dc.contributor.authorSullivan, Robert K. P.en
dc.contributor.authorMichell, Craig T.en
dc.contributor.authorMountford, Jessica K.en
dc.contributor.authorCollin, Shaun P.en
dc.contributor.authorIrigoien, Xabieren
dc.contributor.authorKaartvedt, Steinen
dc.contributor.authorMarshall, Justinen
dc.date.accessioned2017-11-23T11:51:29Z-
dc.date.available2017-11-23T11:51:29Z-
dc.date.issued2017-11-09en
dc.identifier.citationDe Busserolles F, Cortesi F, Helvik JV, Davies WIL, Templin RM, et al. (2017) Pushing the limits of photoreception in twilight conditions: The rod-like cone retina of the deep-sea pearlsides. Science Advances 3: eaao4709. Available: http://dx.doi.org/10.1126/sciadv.aao4709.en
dc.identifier.issn2375-2548en
dc.identifier.doi10.1126/sciadv.aao4709en
dc.identifier.urihttp://hdl.handle.net/10754/626202-
dc.description.abstractMost vertebrates have a duplex retina comprising two photoreceptor types, rods for dim-light (scotopic) vision and cones for bright-light (photopic) and color vision. However, deep-sea fishes are only active in dim-light conditions; hence, most species have lost their cones in favor of a simplex retina composed exclusively of rods. Although the pearlsides, Maurolicus spp., have such a pure rod retina, their behavior is at odds with this simplex visual system. Contrary to other deep-sea fishes, pearlsides are mostly active during dusk and dawn close to the surface, where light levels are intermediate (twilight or mesopic) and require the use of both rod and cone photoreceptors. This study elucidates this paradox by demonstrating that the pearlside retina does not have rod photoreceptors only; instead, it is composed almost exclusively of transmuted cone photoreceptors. These transmuted cells combine the morphological characteristics of a rod photoreceptor with a cone opsin and a cone phototransduction cascade to form a unique photoreceptor type, a rod-like cone, specifically tuned to the light conditions of the pearlsides' habitat (blue-shifted light at mesopic intensities). Combining properties of both rods and cones into a single cell type, instead of using two photoreceptor types that do not function at their full potential under mesopic conditions, is likely to be the most efficient and economical solution to optimize visual performance. These results challenge the standing paradigm of the function and evolution of the vertebrate duplex retina and emphasize the need for a more comprehensive evaluation of visual systems in general.en
dc.description.sponsorshipThis work was supported by King Abdullah University of Science and Technology, the Air Force Office of Scientific Research, and the Australian Research Council via grants awarded to J.M.; a Discovery Project grant (DP140102117) and Future Fellowship (FT110100176) awarded to W.I.L.D.; and a Linkage Infrastructure, Equipment and Facilities (LIEF) grant (LE100100074) awarded to the Queensland Brain Institute (Neurolucida software). F.C. was supported by a Swiss National Science Foundation Early Postdoctoral Mobility Fellowship (165364) and a University of Queensland Development Fellowship. J.V.H. was supported by a start-up grant from the University of Bergen.en
dc.publisherAmerican Association for the Advancement of Science (AAAS)en
dc.relation.urlhttp://advances.sciencemag.org/content/3/11/eaao4709en
dc.rightsThis is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.en
dc.rights.urihttp://creativecommons.org/licenses/by-nc/4.0/en
dc.titlePushing the limits of photoreception in twilight conditions: The rod-like cone retina of the deep-sea pearlsidesen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalScience Advancesen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionQueensland Brain Institute, The University of Queensland, Brisbane, Queensland 4072, Australia.en
dc.contributor.institutionDepartment of Biology, University of Bergen, Bergen 5020, Norway.en
dc.contributor.institutionLions Eye Institute, The University of Western Australia, Crawley, Western Australia 6009, Australia.en
dc.contributor.institutionDepartment of Environmental and Biological Sciences, University of Eastern Finland, Yliopistokatu 7, FI-80101 Joensuu, Finland.en
dc.contributor.institutionIKERBASQUE, Basque Foundation for Science, Bilbao, Spain.en
dc.contributor.institutionDepartment of Biosciences, University of Oslo, Oslo 0316, Norway.en
kaust.authorBusserolles, Fanny deen
All Items in KAUST are protected by copyright, with all rights reserved, unless otherwise indicated.