Visual adaptation in Lake Victoria cichlid fishes: depth-related variation of color and scotopic opsins in species from sand/mud bottoms

Yohey Terai, Ryutaro Miyagi, Mitsuto Aibara, Shinji Mizoiri, Hiroo Imai, Takashi Okitsu, Akimori Wada, Shiho Takahashi-Kariyazono, Akie Sato, Herbert Tichy, Hillary D. J. Mrosso, Semvua I. Mzighani, Norihiro Okada

For Lake Victoria cichlid species inhabiting rocky substrates with differing light regimes, it has been proposed that adaptation of the long-wavelength-sensitive (LWS) opsin gene triggered speciation by sensory drive through color signal divergence. The extensive and continuous sand/mud substrates are also species-rich, and a correlation between male nuptial coloration and the absorption of LWS pigments has been reported. However, the factors driving genetic and functional diversity of LWS pigments in sand/mud habitats are still unresolved. To address this issue, nucleotide sequences of eight opsin genes were compared in ten Lake Victoria cichlid species collected from sand/mud bottoms. Among eight opsins, the LWS and rod-opsin (RH1) alleles were diversified and one particular allele was dominant or fixed in each species. Natural selection has acted on and fixed LWS alleles in each species. The functions of LWS and RH1 alleles were measured by absorption of reconstituted A1- and A2-derived visual pigments. The absorption of pigments from RH1 alleles most common in deep water were largely shifted toward red, whereas those of LWS alleles were largely shifted toward blue in both A1 and A2 pigments. In both RH1 and LWS pigments, A2-derived pigments were closer to the dominant light in deep water, suggesting the possibility of the adaptation of A2-derived pigments to depth-dependent light regimes. The RH1 and LWS sequences may be diversified for adaptation of A2-derived pigments to different light environments in sand/mud substrates. Diversification of the LWS alleles may have originally taken place in riverine environments, with a new mutation occurring subsequently in Lake Victoria.