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.

Highlights

  • Mammals are arguably the most ecologically diverse group of vertebrates, having radiated to fill a diverse range of niches from the deep ocean to the night sky

  • We undertook phylogenetic and molecular analyses of fifty-nine species of mammal to test whether visual adaptation to low light conditions is associated with molecular adaptation in the rod pigment rhodopsin

  • Our analyses included the members of several clades that have independently switched to different forms of ecological niche characterized by low light, including cetaceans, pinnipeds, bats and subterranean mole-rats, as well as the West Indian manatee, Hottentot golden mole and sea otter

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Summary

Introduction

Mammals are arguably the most ecologically diverse group of vertebrates, having radiated to fill a diverse range of niches from the deep ocean to the night sky. Such diversification has involved considerable adaptive changes in their sensory systems. It is perhaps unsurprising that the visual systems of mammals show numerous adaptations for inhabiting different light conditions Such specializations include the anatomical divergence of the lens, iris, pupil and cornea [6,7], the presence of a reflective layer, and the distribution, combination and properties of the constituent light sensitive pigments [8,9]. The SWS1 (shortwavelength sensitive type 1) and M/LWS (middle/long-wavelength sensitive) are restricted to cone photoreceptor cells and are typically responsible for color vision in bright light [8,11], whereas rhodopsin occurs on the rod cells and is extremely sensitive, so enabling dim light (scotopic) vision [8,9]

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