Rapid evolution of cone identity and retinal topography in deep-water crater lake cichlids

Abstract

Deep-water habitats have been colonized repeatedly by fishes, driving the evolution of visual systems under extremely low-light conditions. Here, we investigated visual adaptation in cichlids from the Barombi Mbo crater lake by comparing shallow- and deep-water species using retinal single-cell transcriptomics and analyses of retinal specializations. The shallow-water species Pungu maclareni expressed a broader repertoire of visual opsins across distinct populations of short- (SWS), medium- (RH2), and long-wavelength-sensitive (LWS) cone photoreceptors. In contrast, the deep-water species Myaka myaka lacked a distinct LWS cone population and instead relied predominantly on RH2A/{beta}-expressing, green-sensitive photoreceptors. To assess whether these deep-water RH2 cones corresponded to canonical RH2 or LWS programmes, we compared conserved photoreceptor markers. Deep-water RH2 cones retained elements of both RH2- and LWS-associated transcriptional programmes, revealing a mixed profile lacking a clear canonical cone-type signature. LWS-associated transcriptional regulators also differed between species, with tbx2a absent from M. myaka cones, consistent with the loss of LWS opsin expression, whereas thrb persisted in M. myaka RH2 cones. We further examined retinal specialization across eight species from the radiation and found that retinal topography also differed in photoreceptor distributions and ganglion cell-based acuity centers in association with habitat depth but also with trophic ecology of the species. Together, our findings show that visual adaptation in a young adaptive radiation involves coordinated changes in visual opsin expression, cone-associated transcriptional programmes, and retinal organization, highlighting how sensory systems can quickly evolve through changes at multiple biological levels in response to ecological conditions.