Thyroid hormone tinkering elicits integrated phenotypic changes potentially explaining rapid adaptation of color vision in cichlid fish

Abstract

Vision is critical for most vertebrates, including fish. One challenge that aquatic habitats pose is the high variability in spectral properties depending on depth and the inherent optical properties of the water. By altering opsin gene expression and chromophore usage, cichlid fish modulate visual sensitivities to maximize sensory input from the available light in their respective habitat. Thyroid hormone (TH) has been proposed to play a role in governing adaptive diversification in visual sensitivity in Nicaraguan Midas cichlids, which evolved in less than 4,000 generations. As suggested by indirect measurements of TH levels (i.e., expression of deiodinases), populations adapted to short wavelength light in clear lakes have lower TH levels than ones inhabiting turbid lakes enriched in long-wavelength light. We experimentally manipulated TH levels by exposing two-week-old Midas cichlids to exogenous TH or a TH-inhibitor and measured opsin gene expression and chromophore usage (via cyp27c1 expression). Whereas exogenous TH induces long-wavelength sensitivity by changing opsin gene expression and chromophore usage in a concerted manner, TH-inhibited fish exhibit a visual phenotype with sensitivities shifted to shorter-wavelengths. Tinkering with TH levels in eyes results in concerted phenotypic changes that can provide a rapid mechanism of adaptation to novel light environments.