Light environment and seasonal variation in the visual system of the red shiner (Cyprinella lutrensis)

Abstract

The light environment underwater can vary dramatically over space and time, challenging the visual systems of aquatic organisms. To meet these challenges, many species shift their spectral sensitivities through changes in visual pigment chromophore and opsin expression. The red shiner (Cyprinella lutrensis) is a cyprinid minnow species that has rapidly expanded its range throughout North America and inhabits a wide range of aquatic habitats. We hypothesized that visual system plasticity has contributed to the red shiner's success. We investigated plasticity in chromophore usage and opsin expression by collecting red shiners from three Oklahoma creeks that vary in turbidity throughout the year. We characterized the light environment by spectroradiometry, measured chromophore composition of the eyes with high performance liquid chromatography, characterized CYP27C1 enzyme function through heterologous expression, and examined ocular gene expression by RNA sequencing and de novo transcriptome assembly. We observed significantly higher proportions of the long-wavelength shifted A2 chromophore in the eyes of fish from the turbid site and in samples collected in winter, suggesting that there may be a temperature-dependent trade-off between chromophore-based spectral tuning and chromophore-related noise. Opsin expression varied between turbid and clear creeks, but did not align with light environment as expected, and the magnitude of these differences was limited compared to the differences in chromophore composition. We confirmed that red shiner CYP27C1 catalyzes the conversion of A1 to A2, but the ocular expression of CYP27C1 was not well correlated with A2 levels in the eye, suggesting conversion may be occurring outside of the eye.