Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors

Abstract

SUMMARYVertebrate colour vision is mediated by the differential expression of visual pigment proteins (opsins) in retinal cone photoreceptors. Many species alter opsin expression during life, either as part of development or as a result of changes in habitat. The latter, a result of phenotypic plasticity, appears common among fishes, but its cellular origin and ecological significance are unknown. Here, we used adult threespine stickleback fish from different photic regimes to investigate heritable variability and phenotypic plasticity in opsin expression. Fish from clear waters had double cones that expressed long (LWS) and middle (RH2) wavelength opsins, one per double cone member. In contrast, fish from red light-shifted lakes had double cones that were >95% LWS/LWS pairs. All fish had single cones that predominantly expressed a short wavelength (SWS2) opsin but ultraviolet cones, expressing a SWS1 opsin, were present throughout the retina. Fish from red light-shifted lakes, when transferred to clear waters, had a ~2% increase in RH2/LWS double cones, though double cone density remained constant. Comparison of visual pigment absorbance and light transmission in the environment indicated that the opsin complements of double cones maximized sensitivity to the background light, whereas single cones had visual pigments that were spectrally offset from the dominant background wavelengths. Our results indicate that phenotypic plasticity in opsin expression is minor in sticklebacks and of questionable functional significance. Supplementary material available online at

Rapid adaptive evolution of colour vision in the threespine stickleback radiation

“…The potentially maladaptive shifts seen when substituting to A 2 are a result of overshooting long-wavelength sensitivity relative to the prevalence of these wavelengths in the surveyed freshwater lakes. This finding is consistent with work suggesting A 2 -dominated retinas are common for threespine stickleback from dystrophic lakes that are strongly red-shifted relative to the marine environment, as A 2 use in such an environment would probably result in shifts in an adaptive direction [24].…”

Developmental plasticity in vision and behavior may help guppies overcome increased turbidity

“…Such a rearrangement of the opsin composition in the retina paired with the potential of behavioral compensation for decreased visual fields (i.e., increases in baseline activity) suggest that developmental plasticity in turbid water may allow for greater phenotypic integration in turbid water than activational plasticity would allow for alone. Furthermore, research using three-spined sticklebacks reveals that opsin expression, while developmentally plastic, is not plastic during adulthood (Flamarique et al 2013; similar research with guppies, however, has not been conducted). This relates to the idea that phenotypes may be more costly to change once developed (DeWitt et al 1998), explaining why cues received earlier in development result in a greater range of integration for adult phenotypes.…”

Role of the iridescent eye in stickleback female mate choice

“…The dystrophic lakes have no transmission below 500nm at 1m depth and no light at 4m depth , whereas the mesotrophic systems are characterized by a full light spectrum in surface waters (320-750nm) and peak transmission in the range 560-565nm with depth (Novales Flamarique and Hawryshyn, 1993;Novales Flamarique et al, 2013). Swan Lake exhibits a full light spectrum (320-750nm) in surface waters but is long wavelength dominated with depth Novales Flamarique et al, 2013). During the reproductive season, stickleback nests are found near the shores of these water bodies spanning a ~0.1-1m depth range.…”