Epistatic Adaptive Evolution of Human Color Vision: e1004884

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...

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Bibliographic Details
Published in:PLoS genetics 2014-12, Vol.10 (12)
Main Authors: Yokoyama, Shozo, Xing, Jinyi, Liu, Yang, Faggionato, Davide, Altun, Ahmet, Starmer, William T
Format: Article
Language:English
Subjects:
Amino acids
Colleges & universities
Crystal structure
Evolution & development
Experiments
Eyes & eyesight
Genetic engineering
Genotype & phenotype
Mammals
Mutagenesis
Nitrogen
Phylogenetics
Physiology
Pigments
Proteins
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Summary: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.
ISSN:1553-7390
1553-7404
DOI:10.1371/journal.pgen.1004884