Rhodopsin Molecular Evolution in Mammals Inhabiting Low Light Environments

Abstract

The ecological radiation of mammals to inhabit a variety of light environments is largely attributed to adaptive changes in their visual systems. Visual capabilities are conferred by anatomical features of the eyes as well as the combination and properties of their constituent light sensitive pigments. To test whether evolutionary switches to different niches characterized by dim-light conditions coincided with molecular adaptation of the rod pigment rhodopsin, we sequenced the rhodopsin gene in twenty-two mammals including several bats and subterranean mole-rats. We compared these to thirty-seven published mammal rhodopsin sequences, from species with divergent visual ecologies, including nocturnal, diurnal and aquatic groups. All taxa possessed an intact functional rhodopsin; however, phylogenetic tree reconstruction recovered a gene tree in which rodents were not monophyletic, and also in which echolocating bats formed a monophyletic group. These conflicts with the species tree appear to stem from accelerated evolution in these groups, both of which inhabit low light environments. Selection tests confirmed divergent selection pressures in the clades of subterranean rodents and bats, as well as in marine mammals that live in turbid conditions. We also found evidence of divergent selection pressures among groups of bats with different sensory modalities based on vision and echolocation. Sliding window analyses suggest most changes occur in transmembrane domains, particularly obvious within the pinnipeds; however, we found no obvious pattern between photopic niche and predicted spectral sensitivity based on known critical amino acids. This study indicates that the independent evolution of rhodopsin vision in ecologically specialised groups of mammals has involved molecular evolution at the sequence level, though such changes might not mediate spectral sensitivity directly.

Adaptations to a Subterranean Environment and Longevity Revealed by the Analysis of Mole Rat Genomes

“…Positive selection of the rhodopsin gene ( RHO ), which enables dim light vision, was found in the lineage leading to the common ancestor of DMR and NMR (Table S3). This is consistent with accelerated evolution of African mole rat RHO , while preserving sites critical for spectral tuning (Zhao et al, 2009). Interestingly, we observed cataracts in all examined NMRs ranging from 4 to 20 years of age (Figure S2A).…”

Dark Matters: The Effects of Artificial Lighting on Bats

“…As for most nocturnal mammals, bat retinas are dominated by rods: they are highly sensitive under low light and confer monochromatic vision. The opsin DNA sequences of rhodopsin (the opsin in rods) were intact in 15 bat species (Zhao et al 2009a) and wavelengths of maximum absorbance were 497-501 nm.…”

The fibrous tapetum of the horse eye

“…Rods contribute to visual sensitivity in mesopic and scotopic vision, M/L cones to visual resolution and color vision in photopic vision, and S cones to color vision in photopic vision. In horses, the wavelength of maximum absorption of the rod photopigment is predicted to be 499 nm (Zhao et al 2009), and the spectral peak of cone photopigment sensitivity is 539 nm for M/L cones and 428 nm for S cones (Carroll et al 2001). Therefore, the horizontal band of the tapetum would effectively reflect light that is usable by rod photopigment, and thus increase the sensitivity of mesopic and scotopic vision.…”