TY - JOUR
T1 - Pushing the limits of photoreception in twilight conditions: The rod-like cone retina of the deep-sea pearlsides
AU - Busserolles, Fanny de
AU - Cortesi, Fabio
AU - Helvik, Jon Vidar
AU - Davies, Wayne I. L.
AU - Templin, Rachel M.
AU - Sullivan, Robert K. P.
AU - Michell, Craig T.
AU - Mountford, Jessica K.
AU - Collin, Shaun P.
AU - Irigoien, Xabier
AU - Kaartvedt, Stein
AU - Marshall, Justin
N1 - KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: 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.
PY - 2017/11/8
Y1 - 2017/11/8
N2 - 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.
AB - 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.
UR - http://hdl.handle.net/10754/626202
UR - http://advances.sciencemag.org/content/3/11/eaao4709
UR - http://www.scopus.com/inward/record.url?scp=85041928321&partnerID=8YFLogxK
U2 - 10.1126/sciadv.aao4709
DO - 10.1126/sciadv.aao4709
M3 - Article
C2 - 29134201
SN - 2375-2548
VL - 3
SP - eaao4709
JO - Science advances
JF - Science advances
IS - 11
ER -