Epistatic Adaptive Evolution of Human Color Vision

Abstract

Establishing genotype-phenotype relationship is the key to understand the molecular mechanism of phenotypic adaptation. This initial step may be untangled by analyzing appropriate ancestral molecules, but it is a daunting task to recapitulate the evolution of non-additive (epistatic) interactions of amino acids and function of a protein separately. To adapt to the ultraviolet (UV)-free retinal environment, the short wavelength-sensitive (SWS1) visual pigment in human (human S1) switched from detecting UV to absorbing blue light during the last 90 million years. Mutagenesis experiments of the UV-sensitive pigment in the Boreoeutherian ancestor show that the blue-sensitivity was achieved by seven mutations. The experimental and quantum chemical analyses show that 4,008 of all 5,040 possible evolutionary trajectories are terminated prematurely by containing a dehydrated nonfunctional pigment. Phylogenetic analysis further suggests that human ancestors achieved the blue-sensitivity gradually and almost exclusively by epistasis. When the final stage of spectral tuning of human S1 was underway 45–30 million years ago, the middle and long wavelength-sensitive (MWS/LWS) pigments appeared and so-called trichromatic color vision was established by interprotein epistasis. The adaptive evolution of human S1 differs dramatically from orthologous pigments with a major mutational effect used in achieving blue-sensitivity in a fish and several mammalian species and in regaining UV vision in birds. These observations imply that the mechanisms of epistatic interactions must be understood by studying various orthologues in different species that have adapted to various ecological and physiological environments.

Visual Pigments, Ocular Filters and the Evolution of Snake Vision

“…The T93A substitution found in the vipers Echis ocellatus and Bitis nasicornis has previously been reported but only in the distantly related snake Tropidophis feicki (Simões et al 2015). The precise effects of these substitutions on SWS1 k max are unknown, but substitutions involving sites 86, 93 and 118 in other vertebrates are known to generate substantial shifts in the k max of VS SWS1 pigments (Parry et al 2004;Carvalho et al 2012;Yokoyama et al 2014Carvalho et al 2012.…”

“…Visual pigments play a core role in photon detection and color vision and they are a leading example of how gene duplications (Dulai et al 1999) and changes in amino acid sequences (Yokoyama 2008), type of chromophore (vitamin A 1 or A 2 : Enright et al 2015) and gene expression (Hofmann and Carleton 2009;Carleton et al 2010) underlie adaptations to differing ecological and behavioral selection pressures. Visual opsins in some vertebrates have been studied intensely over the past 20 years, to the extent that changes in specific ("spectral tuning") amino acid sites are known to change the peak absorbance wavelength (k max ) of the visual pigments (Yokoyama 2008;Yokoyama et al 2014). However, there is no universal consensus about the tuning impacts of all such mutations (Hauser et al 2014), with some data suggesting that additional mechanisms to change spectral sensitivity may exist Martin et al 2015).…”

Identifying interesting project phenomena using philosophical and methodological triangulation

“…It can also be explained using the natural science to social science comparative where genes of an organism can not only be switched on and off, but new genes can be created (abet rarely in an evolutionary timeframe), in response to environmental changes (Holliday and Pugh, 1975). For example, for hundreds of thousands of years, our ancestors used to see only in black and white; then with the creation of new genes, our ancestors evolved to have color vision (Yokoyama et al, 2014). The trigger for the creation of new genes was due to changing environmental conditions where plants, trees, and shrubs' started to use color to differentiate their fruits.…”

Molecular evolution of luciferase diversified bioluminescent signals in sea fireflies

“…As phenotypes like color and/or decay evolve, previous changes at certain sites (such as 404) will influence the magnitude of effect new mutations could have. It is also possible that site-specific epistatic interactions changed during the evolution of c-luciferases, as documented in other proteins (Ortlund et al, 2007;Yokoyama et al, 2014) .…”