Mechanisms contributing to opsin expression divergence in the visual system of African Cichlids

Abstract

Vision is an important sensory modality, guiding fundamental tasks such as foraging, escaping from predators, identification of conspecifics and selection of mates. As such, animals exhibit a wide variety of adaptations to spectrally tune their visual systems to closely match the environment. This extensive variation in visual system tuning is achieved both via genetic changes as well as environmental induced plasticity.

Lacustrine cichlids of East Africa are famous for their expedited adaptive radiations. Cichlids in these rift lakes inhabit a diverse range of light environments, from the murky red-shifted waters of Lake Victoria to clear Lake Malawi. Consequently, African cichlids have some of the most diverse visual systems among vertebrates on the planet, with species expressing different combinations of seven cone opsin genes. This differential expression is under genetic control and leads to drastic differences in the visual sensitivities between closely related species. Moreover, cichlid species often exhibit plastic changes in opsin expression due to alterations in environmental light conditions. The diversity of genetically determined visual palettes and the variation in expression due to plastic changes offers an excellent opportunity to study the proximate mechanisms governing opsin expression divergence in this group.

Utilizing a hybrid cross between two species varying in opsin expression, we show that divergent expression of cone opsins is regulated by multiple quantitative trait loci (QTLs). Most of these QTLs are located in trans to the opsins, with the exception of one QTL in cis to the SWS1 opsin. Further fine-mapping of the cis-QTL revealed a deletion in the promoter of the SWS1 gene that is associated with a decrease in its expression. Additionally, performing two reciprocal experiments, we show that adult cichlids from Lake Malawi show rapid and reversible plastic changes in opsin expression due to differences in lighting conditions. These studies show that both predetermined genetic factors and environmental inputs contribute to opsin expression divergence in cichlids. These factors enable short term and ultimately long-term adaptation to changing habitats, facilitating the survival and perhaps speciation of these fantastic fishes.