Pushing the limits of photoreception in twilight conditions: The rod-like cone retina of the deep-sea pearlsides
AuthorsBusserolles, Fanny de
Helvik, Jon Vidar
Davies, Wayne I. L.
Templin, Rachel M.
Sullivan, Robert K. P.
Michell, Craig T.
Mountford, Jessica K.
Collin, Shaun P.
KAUST DepartmentBiological and Environmental Sciences and Engineering (BESE) Division
Red Sea Research Center (RSRC)
Online Publication Date2017-11-08
Print Publication Date2017-11
Permanent link to this recordhttp://hdl.handle.net/10754/626202
MetadataShow full item record
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.
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.
SponsorsThis 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.
Except where otherwise noted, this item's license is described as This 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.
- Phosphorylation-independent suppression of light-activated visual pigment by arrestin in carp rods and cones.
- Authors: Tomizuka J, Tachibanaki S, Kawamura S
- Issue date: 2015 Apr 10
- Ontogenic retinal changes in three ecologically distinct elopomorph fishes (Elopomorpha:Teleostei) correlate with light environment and behavior.
- Authors: Taylor SM, Loew ER, Grace MS
- Issue date: 2015 Jan
- Evolutionary transformation of rod photoreceptors in the all-cone retina of a diurnal garter snake.
- Authors: Schott RK, Müller J, Yang CG, Bhattacharyya N, Chan N, Xu M, Morrow JM, Ghenu AH, Loew ER, Tropepe V, Chang BS
- Issue date: 2016 Jan 12
- The topography of rod and cone photoreceptors in the retina of the ground squirrel.
- Authors: Kryger Z, Galli-Resta L, Jacobs GH, Reese BE
- Issue date: 1998 Jul-Aug
- The two-step development of a duplex retina involves distinct events of cone and rod neurogenesis and differentiation.
- Authors: Valen R, Eilertsen M, Edvardsen RB, Furmanek T, Rønnestad I, van der Meeren T, Karlsen Ø, Nilsen TO, Helvik JV
- Issue date: 2016 Aug 15