Geographic variation in opsin expression does not align with opsin genotype in Lake Victoria cichlid populations

Sensory adaptation to the local environment can contribute to speciation. Aquatic environments are well suited for studying this process: The natural attenuation of light through water results in heterogeneous light environments, to which vision-dependent species must adapt for communication and survival. Here, we study visual adaptation in sympatric Pundamilia cichlids from southeastern Lake Victoria. Species with blue or red male nuptial coloration co-occur at many rocky islands but tend to be depth-differentiated, entailing different visual habitats, more strongly at some islands than others. Divergent visual adaptation to these environments has been implicated as a major factor in the divergence of P. pundamilia and P. nyererei, as they show consistent differentiation in the long-wavelength-sensitive visual pigment gene sequence (LWS opsin). In addition to sequence variation, variation in the opsin gene expression levels may contribute to visual adaptation. We characterized opsin gene expression and LWS genotype across Pundamilia populations inhabiting turbid and clear waters, to examine how different mechanisms of visual tuning contribute to visual adaptation. As predicted, the short-wavelength-sensitive opsin (SWS2b) was expressed exclusively in a population from clear water. Contrary to prediction however, expression levels of the other opsins were species- and island-dependent and did not align with species differences in LWS genotype. Specifically, in two locations with turbid water, the shallow-water dwelling blue species expressed more LWS and less RH2A than the deeper-dwelling red species, while the opposite pattern occurred in the two locations with clear water. Visual modeling suggests that the observed distribution of opsin expression profiles and LWS genotypes does not maximize visual performance, implying the involvement of additional visual tuning mechanisms and/or incomplete adaptation.

This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://hdl.handle.net/10411/I1IUUQ.