Light environment change induces differential expression of guppy opsins in a multi‐generational evolution experiment

Abstract

Light environments critically impact species that rely on vision to survive and reproduce. Animal visual systems must accommodate changes in light that occur from minutes to years, yet the mechanistic basis of their response to spectral (color) changes is largely unknown. Here, we used a laboratory experiment where replicate guppy populations were kept under three different light environments for up to 8-12 generations to explore possible differences in the expression levels of nine guppy opsin genes. Previous evidence for opsin expression-light environment "tuning" has been either correlative or focused exclusively on the relationship between the light environment and opsin expression over one or two generations. In our multigeneration experiment, the relative expression levels of nine different guppy opsin genes responded differently to light environment changes: some did not respond, while others differed due to phenotypic plasticity. Moreover, for the LWS-1 opsin we found that, while we observed a wide range of plastic responses under different light conditions, common plastic responses (where the population replicates all followed the same trajectory) occurred only after multigenerational exposure to different light environments. Taken together this suggests that opsin expression plasticity plays an important role in light environment "tuning" in different light environments on different time scales, and, in turn, has important implications for both visual system function and evolution.

Colour‐based foraging diverges after multiple generations under different light environments

“…The blue and blue‐green stimuli in our study stimulate both short and medium wavelength guppy cones. Kranz, Forgan et al () found no variation in short wavelength opsin expression across light environments but a decrease in medium wavelength opsin expression when fish were moved from the green and lilac environments to the same light environment as our test conditions (Kranz, Forgan et al, ). The relative expression of opsins has been shown to influence colour‐based behaviours (Smith, Ma, Soares, & Carleton, ), and thus, changes in the medium wavelength opsin expression of the fish may explain the decrease in pecking behaviour towards the blue and blue‐green stimuli.…”

“…The green stimulus was the only stimulus to be pecked at consistently across all treatments and replicates. The medium wavelength sensitive cones that are most highly stimulated by the green stimulus have the same expression across the three treatments as shown by Kranz, Forgan et al (2018b). There is also little difference in the position of the green stimulus in guppy tetrahedral colour space, indicating that this colour would be perceived similarly across all light treatments.…”

“…These colours are partially detected by the long wavelength opsins for which guppies are known to be polymorphic (Archer et al, 1987;Archer & Lythgoe, 1990). In a previous study, guppy populations from the same green light treatment showed changes in expression over time with differences in expression between replicate green populations probably due to different timing in plastic response (Kranz, Forgan et al, 2018b). It is possible that these differences in opsin expression between the green replicate populations have resulted in the behavioural differences that we see between the green replicate treatments towards the red stimuli.…”

Altered visual environment affects a tropical freshwater fish assemblage through impacts on predator–prey interactions

“…In other ecosystems, the introduction of artificial light at night can increase the duration of feeding times for visual predators, alter prey densities (e.g. Torres-Dowdall et al 2012;Kranz et al 2018;Ehlman, Martinez & Sih 2018) Gordon et al 2015). Changes in visual environments that might affect the efficacy of camouflage (e.g.…”

Colour pattern component phenotypic divergence can be predicted by the light environment

“…The irradiance spectra of these three light treatments were recorded by an Ocean Optics USB2000+ spectrometer calibrated for photon flux (visually relevant units, lmol photons m À1 s À1 nm À1 ) with a Li-Cor LI-1800-02 optical radiation calibrator. These three filter treatments were selected to be similar to different natural light environments (Endler, 1993b;Kranz et al, 2018). Green-F89 are more similar to forest shade natural light environments (Endler, 1993b).…”