Widespread and Convergent Evolution of Cone Monochromacy in Galeomorph Sharks.

Abstract

Color vision is widespread in marine vertebrates but is notably lacking in whales, dolphins, seals, and apparently also sharks. All sharks studied to date possess only a single spectral class of cone and are thus potentially totally color blind. The reason why sharks lack color vision is unclear, but as the visual pigments of only a handful of this large and ecologically diverse taxon have been studied, more data are required to address this question. Here, we assembled the retinal transcriptomes of 9 species from 7 families and 3 orders within the superorder Galeomorphii to screen for visual opsin and phototransduction genes. We reveal that cone monochromacy is widespread in galeomorph sharks, but the type of cone opsin expressed varies, with lamniform and orectolobiform sharks expressing a long-wavelength-sensitive (LWS) opsin, and carcharhiniform and heterodontiform sharks expressing a rhodopsin-like 2 (RH2) opsin. Cone monochromacy has evolved from a dichromatic ancestral state at least 4 times, implying strong selection pressure to prioritize achromatic over chromatic vision. While all species express the GRK1A and GRK7 isoforms of G protein-coupled receptor kinase, only sharks with the LWS cone opsin express the GRK1B isoform, which suggests that nonspectral functions of photoreception may have influenced, or result from, the opsin complement in the shark retina. Finally, we show that the shark rod (RH1) opsin gene shows evidence of positive selection at sites known to influence pigment kinetics (i.e. metarhodopsin II stability) and that the rate of retinal release likely differs substantially between species in ways that reflect their physiology and ecology.