title: Adaptive evolutionary paths from UV reception to sensing violet light by epistatic interactions.
abstract: Ultraviolet (UV) reception is useful for such basic behaviors as mate choice, foraging, predator avoidance, communication, and navigation, whereas violet reception improves visual resolution and subtle contrast detection. UV and violet reception are mediated by the short wavelength-sensitive (SWS1) pigments that absorb light maximally (λmax) at ~360 nm and ~395 to 440 nm, respectively. Because of strong nonadditive (epistatic) interactions among amino acid changes in the pigments, the adaptive evolutionary mechanisms of these phenotypes are not well understood. Evolution of the violet pigment of the African clawed frog (Xenopus laevis, λmax = 423 nm) from the UV pigment in the amphibian ancestor (λmax = 359 nm) can be fully explained by eight mutations in transmembrane (TM) I-III segments. We show that epistatic interactions involving the remaining TM IV-VII segments provided evolutionary potential for the frog pigment to gradually achieve its violet-light reception by tuning its color sensitivity in small steps. Mutants in these segments also impair pigments that would cause drastic spectral shifts and thus eliminate them from viable evolutionary pathways. The overall effects of epistatic interactions involving TM IV-VII segments have disappeared at the last evolutionary step and thus are not detectable by studying present-day pigments. Therefore, characterizing the genotype-phenotype relationship during each evolutionary step is the key to uncover the true nature of epistasis.
authors.affiliation: Department of Biology, Emory University, Atlanta, GA 30322, USA.
authors.forename: Shozo
authors.initials: S
authors.lastname: Yokoyama
authors.affiliation: Department of Physics and Department of Genetics and Bioengineering, Fatih University, Istanbul 34500, Turkey.
authors.forename: Ahmet
authors.initials: A
authors.lastname: Altun
authors.affiliation: Department of Biology, Emory University, Atlanta, GA 30322, USA.
authors.forename: Huiyong
authors.initials: H
authors.lastname: Jia
authors.affiliation: Department of Biology, Emory University, Atlanta, GA 30322, USA.
authors.forename: Hui
authors.initials: H
authors.lastname: Yang
authors.affiliation: Department of Biology, Emory University, Atlanta, GA 30322, USA.
authors.forename: Takashi
authors.initials: T
authors.lastname: Koyama
authors.affiliation: Department of Biology, Emory University, Atlanta, GA 30322, USA.
authors.forename: Davide
authors.initials: D
authors.lastname: Faggionato
authors.affiliation: Department of Biology, Emory University, Atlanta, GA 30322, USA.
authors.forename: Yang
authors.initials: Y
authors.lastname: Liu
authors.affiliation: Department of Biology, Syracuse University, Syracuse, NY 13244, USA.
authors.forename: William T
authors.initials: WT
authors.lastname: Starmer
keywords: UV reception; adaptive mutations; ancestral amino acids; chemical impairments; epistatic interactions; evolutionary trajectories; mutagenesis experiments; vertebrates; violet reception; visual pigments