Seeing in the deep: evolution of the opsin gene expression in Bermin crater lake cichlids

Abstract

Cichlid visual systems can evolve rapidly during adaptive radiations. This study investigates the Bermin crater lake species flock in Cameroon, comprising thirteen (nine valid and four undescribed) Coptodon species, to explore the effects of deep-water light environments on visual evolution. We analyzed visual opsin genes and their expression using 109 retina transcriptomes, focusing on differences among species at varying depths, and seasonal changes in the visual system of a seasonally migrating species. All species exhibit a multichromatic system with at least five cone opsins. While opsin sequence variability among species was minimal due to the flocks evolutionary youth, opsin expression patterns varied significantly. Deep-water species showed reduced SWS1 and SWS2B expression, consistent with diminished UV-to-violet light in deeper waters. Unexpectedly, we observed increased proportional expression of the red-sensitive LWS opsin gene, contrary to trends seen in other lacustrine fishes. Additionally, in the seasonally deep-dwelling species Coptodon imbriferna, opsin expression varied plastically between the rainy (shallow) and dry (deep) seasons, with reduced SWS2B expression when the fish reside in the deeper habitats. To add context of other cichlid systems and to explore shared patterns of molecular adaptation, we compared Bermin cichlids to the deep-water species of the Barombi Mbo crater lake. Both cases exemplify independent evolution of deep-water species, yet their visual systems adapted similarly in the single cones (less UV- and violet-sensitive and more blue-sensitive cones), whereas differently in the long-wavelength sensitive double cones (LWS expression lost in Barombi while increased in Bermin). Overall, our study focuses on an evolutionarily young example of cichlid adaptive radiation, providing a unique opportunity to examine the initial phases of molecular adaptation in visual systems.