Opsin gene evolution in amphibious and terrestrial combtooth blennies (Blenniidae)

Abstract

Evolutionary adaptations to life on land include changes to the physiology, morphology and behaviour of an animal in response to physical differences between water and air. The visual systems of amphibious species show pronounced morphological adaptations; yet, whether molecular changes also occur remains largely unknown. Here, we investigated the molecular evolution of visual pigment genes (opsins) in amphibious and terrestrial fishes belonging to the Salariini division of blennies (Blenniidae). We hypothesized that when conquering land, blenny opsins adapt - in terms of sequence variation and/or gene expression - to match both higher light intensities as well as the broader light spectrum. Using retinal transcriptomes in six species ranging from fully aquatic to fully terrestrial, we found very little variation in opsin gene sequences or gene expression between species. All blennies expressed a single rod opsin gene as well as two cone opsin genes sensitive to longer-wavelengths of light: RH2A-1 (green-sensitive) and LWS (red-sensitive). They also expressed one or two short-wavelength-sensitive cone opsin genes (SWS2A, SWS2A{beta}; blue-sensitive) in a phylogenetically inert manner. However, based on amino acid predictions, both SWS2A proteins confer similar peak spectral sensitivities and differential expression is therefore unlikely to be ecologically significant. Red-sensitivity is likely beneficial for feeding on algae and detritus, the main food source of Salariini blennies, and could be co-adapted to perceive visual displays in terrestrial species, which often use red dorsal fins to signal during aggressive disputes and courtship. Our data suggests that on the molecular level, the visual systems that evolved in aquatic blennies have been retained in species that have transitioned onto land.