Short term colour vision plasticity on the reef: Changes in opsin expression under varying light conditions differ between ecologically distinct reef fish species

Abstract

Vision mediates important behavioural tasks such as mate choice, escape from predators and foraging. In fish, photoreceptors are generally tuned to specific visual tasks and/or to their light environment, according to depth or water colour to ensure optimal performance. Evolutionary mechanisms acting on genes encoding opsin, the protein component of the photopigment, can influence the spectral sensitivity of photoreceptors. Opsin genes are known to respond to environmental conditions on a number of time scales, including short time frames due to seasonal variation, or through longer-term evolutionary tuning. There is also evidence for 'on-the-fly' adaptations in adult fish in response to rapidly changing environmental conditions; however, results are contradictory. Here, we investigated the ability of three reef fish species that belong to two ecologically distinct families, yellow-striped cardinalfish (), Ambon damselfish () and lemon damselfish (), to alter opsin gene expression as an adaptation to short-term (weeks to months) changes of environmental light conditions, and attempted to characterize the underlying expression regulation principles. We report the ability for all species to alter opsin gene expression within months and even a few weeks, suggesting that opsin expression in adult reef fish is not static. Furthermore, we found that changes in opsin expression in single cones generally occurred more rapidly than in double cones, and identified different responses of opsin gene expression between the ecologically distinct reef fish families. Quantum catch correlation analysis suggested different regulation mechanisms for opsin expression dependent on gene class.

Colours and colour vision in reef fishes: Past, present and future research directions

“…() found that placing pomacentrids and apogonids into tanks with different red, green or blue lighting results in plastic adaptations in opsin gene expression. Interestingly, while pomacentrids mostly adjusted the expression of their single cone opsins ( SWS1 and SWS2 ), the apogonids showed the greatest plasticity in their double cone genes ( RH2 and LWS ) (Luehrmann et al ., ) this making some sense as apogonids are primarily nocturnal and may need greater plasticity in their more sensitive double cones. Several reef‐fishes are furthermore known to exist over substantial depth ranges where ambient illumination may differ greatly.…”

“…Also, marine fishes such as the yellowfin tuna Thunnus albacares (Bonnaterre 1788) (Loew et al ., ) and starry flounder, Platichthys stellatus (Pallas 1787) (Savelli et al ., ) co‐express multiple opsin pigments during development, but the functionality of this remains elusive. Co‐expression of visual pigments seems a prominent feature of many reef fishes also with detailed studies in pseudochromids and P. leopardus (Cortesi et al ., 2016), opmacentrids (Luehrmann et al ., ), and squirrelfishes (Holocentrinae; F. de Busserolles, N.J. Marshall, & S.P. Collin, unpublished data).…”

“…Dorso‐ventrally divided retinas are common in marine fishes often with more double cones looking downwards, presumably to boost sensitivity if indeed they do act as daytime luminance detectors. Single cones, including those with UV sensitivity are more frequent medially and ventrally in some species of fish (Luehrmann et al ., ), presumably, like mice that share this zonation plan, to look into the UV‐rich visual world from above (Peichl, ).…”

“…; and for explanation of retinal maps such as these see de Busserolles et al (2014) 3.5 | Spectral sensitivity change -short-term Shorter-term spectral shifts have been noted where fishes are kept under different lighting regimes in the lab or where for instance, seasonal difference in light environments exist (Bowmaker, 2008;Bowmaker and Loew, 2007;Stieb et al, 2017). Luehrmann et al (2018) found that placing pomacentrids and apogonids into tanks with different red, green or blue lighting results in plastic adaptations in opsin gene expression. Interestingly, while pomacentrids mostly adjusted the expression of their single cone opsins (SWS1 and SWS2), the apogonids showed the greatest plasticity in their double cone genes (RH2 and LWS) (Luehrmann et al, 2018) this making some sense as apogonids are primarily nocturnal and may need greater plasticity in their more sensitive double cones.…”

Diurnal variation in opsin expression and common housekeeping genes necessitates comprehensive normalization methods for quantitative real‐time PCR analyses

“…The particular methods used to normalize opsin expression are important because there is incredible variation in opsin expression across animals depending on the time of day (Halstenberg et al, ; Johnson et al, ; Korenbrot & Fernald, ; Li et al, ; Pierce et al, ; von Schantz et al, ), genetic variation and species differences (Fuller, Carleton, Fadool, Spady, & Travis, ; O’Quin et al, ), developmental stage (Carleton et al, ; Cheng & Flamarique, ; Roberts, Srinivas, Forrest, Escobar, & Reh, ), and plastic response to environmental changes (Everett, Tong, Briscoe, & Monteiro, ; Fuller & Claricoates, ; Hofmann, O’Quin, Smith, & Carleton, ; Luehrmann et al, ; Stieb, Carleton, Cortesi, Marshall, & Salzburger, ; Valen, Karlsen, & Helvik, ; Veen, Brock, Rennison, & Bolnick, ). There have been five commonly used methods, each with their own merits and drawbacks, to normalize opsin expression for questions of visual ecology and evolution: (a) relative to housekeeping gene expression, (b) relative to total RNA concentration, (c) relative to expression of the cone‐specific alpha subunit of transducin ( GNAT2) , (d) proportion of total pool of opsin expression and (e) relative to pool of opsin expression from the same cone type.…”