Fine‐tuning light sensitivity in the starry flounder (: Regional variation in photoreceptor cell morphology and opsin gene expressionPlatichthys stellatus: Regional variation in photoreceptor cell morphology and opsin gene expression) retina: Regional variation in photoreceptor cell morphology and opsin gene expression

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Opsins are membrane‐bound G‐protein coupled receptors (GPCRs) that form light sensitive visual pigments when bound to a vitamin‐A derived chromophore (Hárosi, 1994; Yokoyama 1997). Although many other opsins (e.g., melanopsin, neuropsin, teleost multi‐tissue opsin) are expressed in visual tissues (Davies et al., 2015; Porter et al., 2011), we use the term “visual opsin” to refer to the five opsin subfamilies commonly associated with vertebrate rods and cones (e.g., RH1, RH2, LWS, SWS1, and SWS2). The ability to detect and discriminate among different wavelengths of light depends on the diversity and distribution of different types of photoreceptors (expressing different opsins) in the retina. Humans, with three different cone opsins, OPN1SW, OPN1MW, and OPN1LW, have trichomatic color vision. Mutations that reduce the number of visual opsins, or sequence diversity among opsins, lead to color vision deficiencies (Jacobs, 2013; Yokoyama, 1997).
Teleost fish typically have many more opsins than other vertebrates (Davies et al., 2015; Rennison, Owens, & Taylor, 2012). For the visual opsins this is largely the result of lineage‐specific tandem duplication events (Chinen, Hamaoka, Yamada, & Kawamura, 2003; Rennison et al., 2012). The adaptive value of such large opsin gene repertoires is unclear. Improved wavelength discrimination is a possible explanation. Humans and other primates with three cone opsins (trichromatic) have better wavelength discrimination than mammals with two cone opsins (dichromatic) (Mancuso et al., 2009; Melin et al., 2009). Adding an opsin to the retinas of dichromatic squirrel monkeys (Mancuso et al., 2009) and mice (Jacobs, Fenwick, Calderone, & Deeb, 1999, 2007) through gene therapy can produce behavior indicative of trichromatic vision. However, chickens, with four cone opsins, do not perform any better than humans in wavelength discrimination tests (Olsson, Lind, & Kelber, 2015). As well, some stomatopod crustaceans have 12 different spectral photoreceptors, but perform poorly in color discrimination tasks; the difference between two wavelengths had to exceed 12–25 nm before stomatopods could successfully discriminate between them (Thoen, How, Chiou, & Marshall, 2014). With three cone opsins humans can discriminate between wavelengths of light that differ by as little as a fraction of a nm in some regions of the spectrum (Mollon, Estévez, & Cavonius, 1990) to a few nm in others (Pokorny & Smith, 1970; Zhaoping, Geisler, & May, 2011).
It is possible that large opsin repertoires allow vision to be tuned to different light environments experienced over varying time scales. Data from multiple species, including Lake Malawi cichlids (Dalton, Lu, Leips, Cronin, & Carleton, 2015; Parry et al., 2005), the dusky dottyback (Cortesi et al., 2015), rainbow trout (Cheng & Novales Flamarique, 2007), guppy (Sakai, Ohtsuki, Kasagi, Kawamura, & Kawata, 2016), and bluefin killifish (Fuller & Claricoates, 2011; Fuller, Carleton, Fadool, Spady, & Travis, 2005) show that opsin expression can change quickly in response to a change in the light environment. In salmonid fishes (Cheng, Novales Flamarique, Hárosi, Rickers‐Haunerland, & Haunerland, 2006) and flatfishes (Evans, Hárosi, & Fernald, 1993), changes in opsin expression may occur gradually, as a function of ontogeny and changing habitats during life history migrations.
Changes in opsin expression may also involve differential opsin expression within the retina (Dalton et al., 2015). Such intraretinal variation is common among vertebrates. For instance, humans and other primates lack Sws1‐expressing cones (S‐cones) in the fovea (Ahnelt, Kolb, & Pflug, 1981; Hagstrom, Neitz, & Neitz, 1998) and mice have opposing ventro‐dorsal retinal gradients of Sws1 and M/Lws opsin expression (Applebury et al., 2000). Many fish species experience a photic environment that varies substantially in intensity and spectral distribution with line of sight, and opsins are sometimes expressed in a pattern indicative of a response to this variation.
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