Retinal specialization through spatially varying cell densities and opsin coexpression in cichlid fish

被引:35
作者
Dalton, Brian E. [1 ]
de Busserolles, Fanny [2 ]
Marshall, N. Justin [2 ]
Carleton, Karen L. [1 ]
机构
[1] Univ Maryland, Dept Biol, College Pk, MD 20742 USA
[2] Univ Queensland, Queensland Brain Inst, Brisbane, Qld 4072, Australia
基金
澳大利亚研究理事会; 美国国家卫生研究院;
关键词
Vision; Retina; Spectral sensitivity; Visual acuity; LAKE MALAWI; CONE PHOTORECEPTOR; INTERSPECIFIC VARIATION; SPECTRAL SENSITIVITY; TYRANT FLYCATCHERS; COLOR-VISION; LAYER; EXPRESSION; DIVERGENCE; MECHANISMS;
D O I
10.1242/jeb.149211
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
The distinct behaviours of animals and the varied habitats in which animals live place different requirements on their visual systems. A trade-off exists between resolution and sensitivity, with these properties varying across the retina. Spectral sensitivity, which affects both achromatic and chromatic (colour) vision, also varies across the retina, though the function of this inhomogeneity is less clear. We previously demonstrated spatially varying spectral sensitivity of double cones in the cichlid fish Metriaclima zebra owing to coexpression of different opsins. Here, we map the distributions of ganglion cells and cone cells and quantify opsin coexpression in single cones to show these also vary across the retina. We identify an area centralis with peak acuity and infrequent coexpression, which may be suited for tasks such as foraging and detecting male signals. The peripheral retina has reduced ganglion cell densities and increased opsin coexpression. Modeling of cichlid visual tasks indicates that coexpression might hinder colour discrimination of foraging targets and some fish colours. But, coexpression might improve contrast detection of dark objects against bright backgrounds, which might be useful for detecting predators or zooplankton. This suggests a trade-off between acuity and colour discrimination in the central retina versus lower resolution but more sensitive contrast detection in the peripheral retina. Significant variation in the pattern of coexpression among individuals, however, raises interesting questions about the selective forces at work.
引用
收藏
页码:266 / 277
页数:12
相关论文
共 55 条
[1]   Ontogeny of Cone Photoreceptor Mosaics in Zebrafish [J].
Allison, W. Ted ;
Barthel, Linda K. ;
Skebo, Kristina M. ;
Takechi, Masaki ;
Kawamura, Shoji ;
Raymond, Pamela A. .
JOURNAL OF COMPARATIVE NEUROLOGY, 2010, 518 (20) :4182-4195
[2]   Transient expression of thyroid hormone nuclear receptor TRβ2 sets S opsin patterning during cone photoreceptor genesis [J].
Applebury, M. L. ;
Farhangfar, F. ;
Glosmann, M. ;
Hashimoto, K. ;
Kage, K. ;
Robbins, J. T. ;
Shibusawa, N. ;
Wondisford, F. E. ;
Zhang, H. .
DEVELOPMENTAL DYNAMICS, 2007, 236 (05) :1203-1212
[3]   The murine cone photoreceptor: A single cone type expresses both S and M opsins with retinal spatial patterning [J].
Applebury, ML ;
Antoch, MP ;
Baxter, LC ;
Chun, LLY ;
Falk, JD ;
Farhangfar, F ;
Kage, K ;
Krzystolik, MG ;
Lyass, LA ;
Robbins, JT .
NEURON, 2000, 27 (03) :513-523
[4]   spatstat: An R package for analyzing spatial point patterns [J].
Baddeley, A ;
Turner, R .
JOURNAL OF STATISTICAL SOFTWARE, 2005, 12 (06) :1-42
[5]   A Tale of Two Retinal Domains: Near-Optimal Sampling of Achromatic Contrasts in Natural Scenes through Asymmetric Photoreceptor Distribution [J].
Baden, Tom ;
Schubert, Timm ;
Chang, Le ;
Wei, Tao ;
Zaichuk, Mariana ;
Wissinger, Bernd ;
Euler, Thomas .
NEURON, 2013, 80 (05) :1206-1217
[6]  
Barthel LK, 2000, METHOD ENZYMOL, V316, P579
[7]   Not all butterfly eyes are created equal:: Rhodopsin absorption spectra, molecular identification, and localization of ultraviolet-, blue-, and green-sensitive rhodopsin-encoding mRNAs in the retina of Vanessa cardui [J].
Briscoe, AD ;
Bernard, GD ;
Szeto, AS ;
Nagy, LM ;
White, RH .
JOURNAL OF COMPARATIVE NEUROLOGY, 2003, 458 (04) :334-349
[8]   Proximate and ultimate causes of variable visual sensitivities: Insights from cichlid fish radiations [J].
Carleton, Karen L. ;
Dalton, Brian E. ;
Escobar-Camacho, Daniel ;
Nandamuri, Pratima .
GENESIS, 2016, 54 (06) :299-325
[9]   Blue and Yellow Signal Cleaning Behavior in Coral Reef Fishes [J].
Cheney, Karen L. ;
Grutter, Alexandra S. ;
Blomberg, Simon P. ;
Marshall, N. Justin .
CURRENT BIOLOGY, 2009, 19 (15) :1283-1287
[10]   The retina of tyrant flycatchers:: Topographic organization of neuronal density and size in the ganglion cell layer of the great kiskadee Pitangus sulphuratus and the rusty margined flycatcher Myiozetetes cayanensis (Aves: Tyrannidae) [J].
Coimbra, Joao Paulo ;
Luiza Videira Marceliano, Maria ;
Lara da Silveira Andrade-da-Costa, Belmira ;
Yamada, Elizabeth Sumi .
BRAIN BEHAVIOR AND EVOLUTION, 2006, 68 (01) :15-25