Rapid Divergence of Visual Systems and Signaling Traits to Contrasting Light Regimes During Early Speciation of African Crater Lake Cichlid Fish

Sensory adaptation is widely hypothesised to drive ecological speciation, yet empirical evidence from natural populations undergoing early-stage divergence remains limited. In Lake Masoko, a young crater lake in East Africa, the haplochromine cichlid Astatotilapia calliptera is undergoing early-stage sympatric speciation into shallow-water littoral and deep-water benthic ecotypes that experience contrasting light environments. Here we integrate retinal transcriptomics, phenotypic analyses, and visual modelling to uncover rapid sensory divergence associated with this ecological transition. We find striking shifts in cone opsin expression, with the benthic ecotype exhibiting a switch from short-wavelength sensitive SWS2B to SWS2A and an overall narrowing of cone sensitivity towards the centre of the light spectrum, consistent with changes in deep-water light environment. In contrast, coding sequence variation in opsin genes was limited and no significant differences in allele frequencies were detected across nine polymorphic sites, pointing to expression regulation as the primary axis of early divergence in visual systems. In parallel, we observed divergence in male signalling traits, with benthic males displaying deeper red egg-spots, aligning with predictions from visual modelling of signal efficiency in different light environments. These results demonstrate rapid transcriptomic and phenotypic divergence in associated signalling traits-within ∼1,000 years-supporting a potential role for regulatory evolution in sensory adaptation during early ecological speciation.