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.

Figure 1. Putative gene tree for rhodopsin using ML and Bayesian approaches with no constraints on the topology.

Branch lengths are scaled by the number of nucleotide substitutions per site. Numbers at the nodes are ML bootstrap values/Bayesian posterior probabilities. 100* represents both 100% ML bootstrap support and a posterior probability of 1. Focal branches examined in our selection tests are shown in red. These comprise the ancestral branches to the high-duty-cycle echolocating bats (HDC), the Yangochiroptera (YAN), the Chiroptera (BAT), the Old World fruit bats (OWF), the cetaceans (CET), the pinnipeds (PIN) the African mole-rats (AFM) as well as to ancestral branches to four individual taxa (sea otter, West Indian manatee, Hottentot golden mole and Middle East blind mole-rat). Within the bats, Yinpterochiroptera is coded as Yi and Yangochiroptera as Ya. In addition, the names of taxa known to have lost their SWS1 opsin are shown in red, and their corresponding photopic niches are colour coded as brown for subterranean and light blue for aquatic. Finally, all bats have been shaded grey.

Figure 2. Sliding window analysis (window size  = 30 bp, step size  = 3 bp) to show variation in omega value (dN/dS) along the rhodopsin gene, between all mammals (black) and, in red, (A) African mole-rats, (B) cetaceans, (C) pinnipeds and (D) bats.

Beneath each plot is a schematic of the rhodopsin gene, which illustrates the distribution of transmembrane domains (black), extracellular (white) and intracellular (grey) domains.