High complexity of aquatic irradiance may have driven the evolution of four-dimensional colour vision in shallow-water fish.

Humans use three cone photoreceptor classes for colour vision, yet many birds, reptiles and shallow-water fish are tetrachromatic and use four cone classes. Screening pigments, which narrow the spectrum of photoreceptors in birds and diurnal reptiles, render visual systems with four cone classes more efficient. To date, however, the question of tetrachromacy in shallow-water fish that, like humans, lack screening pigments, is still unsolved. We raise the possibility that tetrachromacy in fish has evolved in response to higher spectral complexity of underwater light. We compared the dimensionality of colour vision in humans and fish by examining the spectral complexity of the colour signal reflected from objects into their eyes. We show that fish require four to six cone classes to reconstruct the colour signal of aquatic objects at the accuracy level achieved by humans viewing terrestrial objects. This is because environmental light, which alters the colour signals, is more complex and contains more spectral fluctuations underwater than on land. We further show that fish cones are better suited than human cones to detect these spectral fluctuations, suggesting that the capability of fish cones to detect high-frequency fluctuations in the colour signal confers an advantage. Taken together, we propose that tetrachromacy in fish has evolved to enhance the reconstruction of complex colour signals in shallow aquatic environments. Of course, shallow-water fish might possess fewer than four cone classes; however, this would come with the inevitable loss in accuracy of signal reconstruction.