Abstract

Common ancestors of vertebrates had four types of cone opsins: short-wavelength sensitive 1 (SWS1), SWS2, rhodopsin 2 (RH2), and long-wavelength sensitive (LWS) types. Whereas fish and birds retain all the types, mammals have lost two of them (SWS2 and RH2) possibly because of their nocturnal lifestyle during the Mesozoic Era. Considering that the loss of cone opsin types causes so-called color blindness in humans (e.g., protanopia), the ability to discriminate color by trichromatic humans could be lower than that in potentially tetrachromatic birds and fish. Behavioral studies using color-blind (cone opsin-knockout) animals would be helpful to address such questions, but it is only recently that the genome-editing technologies have opened up this pathway. Using medaka as a model, we introduced frameshift mutations in SWS2 (SWS2a and/or SWS2b) after detailed characterization of the loci in silico, which unveiled the existence of a GC–AG intron and non-optic expressed-sequence-tags (ESTs) that include SWS2a in part. Transcripts from the mutated SWS2 loci are commonly reduced, suggesting that the SWS2a/b-double mutants could produce, if any, severely truncated (likely dysfunctional) SWS2s in small amounts. The mutants exhibited weakened body color preferences during mate choice. However, the optomotor response (OMR) test under monochromatic light revealed that the mutants had no defect in spectral sensitivity, even at the absorbance maxima (λmax) of SWS2s. Evolutionary diversification of cone opsins has often been discussed in relation to adaptation to dominating light in habitats (i.e., changes in the repertoire or λmax are for increasing sensitivity to the dominating light). However, the present results seem to provide empirical evidence showing that acquiring or losing a type of cone opsin (or changes in λmax) need not substantially affect photopic or mesopic sensitivity. Other points of view, such as color discrimination of species-specific mates/preys/predators against habitat-specific backgrounds, may be necessary to understand why cone opsin repertories are so various among animals.

Highlights

  • Colors are virtual images evoked in the brain by light spectra received at the retina

  • This database search identified some interesting clones containing a part of the first and the entire second to fifth exons of SWS2a, which are connected to an upstream gene or intergenic regions (Figure 1B)

  • Four types of cone cells are regularly arranged in the fish retina forming the retinal mosaic (Nishiwaki et al, 1997; Allison et al, 2010), but expressions of cone opsins are rather complex; for example, different types of opsins could be coexpressed in a single cone and the expression can change relying on growth stages, ambient light, or visual angles (Dalton et al, 2014; Sakai et al, 2018; Zimmermann et al, 2018)

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Summary

Introduction

Colors are virtual images evoked in the brain by light spectra received at the retina. Light is received by three types (or more precisely, two types with one subtype; see below) of visual pigments (cone opsins) and converted to an electronic signal of three channels (Young, 1802) This signal is converted to a two-dimensional value defined by the red– green and blue–yellow axes (Hering, 1920) via complex neural networks of horizontal, bipolar, amacrine, and ganglion cells (Thoreson and Dacey, 2019), which is sent to the visual cortex of the brain where colors are evoked. This mechanism (still not fully understood, the processing in the brain) will explain color perception only in a part of the Old World monkeys (Catarrhini). The cone cells in their retina are classified morphologically into two types (expressing SWS1 or either of the LWS subtypes), which are arranged largely at random (Viets et al, 2016)

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