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Adaptive evolutionary paths from UV reception to sensing violet light by epistatic interactions.
Yokoyama S
,
Altun A
,
Jia H
,
Yang H
,
Koyama T
,
Faggionato D
,
Liu Y
,
Starmer WT
.
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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.
Fig. 1. Two-dimensional model of AncAmphibian-359.Twelve amino acid changes that shifted the λmax are shown in black (highly critical) and blue (less so). Seven arrowheads indicate restriction recognition sites (fig. S1). The model is after Palczewski (46).
Fig. 2. The absorption spectra of various chimeric pigments that are derived from A2F.The white and black segments of the visual pigment (inset) indicate those of AncAmphibian-359 and frog-423, respectively. The λmaxs of A2F mutants with various amino acid changes are also shown in parentheses.
Fig. 3. The most probable pattern of the amino acid replacements during amphibian pigment evolution.The evolutionary tree of frog-423 and orthologous amphibian pigments, where the divergence times at the three nodes were obtained from the TimeTree of Life web server (www.timetree.org). Six functionally critical amino acid replacements are shown above, where the numbers are the products of the PPs of the two amino acids inferred and indicate the likelihoods that these changes occur at a specific evolutionary stage. The PPs are taken from the maximum likelihood–based Bayesian method (35) with the JTT model, and the logos of amino acids at 12 critical sites for the three ancestral amphibian pigments indicate their support values, where amino acids in red have PPs >0.95 (table S1). Branches and boxes in black and blue indicate UV and violet sensitivities, respectively. Sharing only T118, I207, and T277 among the 12 critical amino acids of frog-423, the bullfrog SWS1 pigment must have achieved its violet sensitivity (55) using an entirely different mechanism. (For the sequence of mutation accumulations, see the “Evolutionary trajectories” section. MYA, million years ago.)
Fig. 4. The tertiary structures of SWS1 pigments.(A) A3F. (B) A34F. (C) A35F. (D) A36F. Black, blue, red, and white molecules represent carbon, nitrogen, oxygen, and hydrogen atoms, respectively.
Fig. 5. All 120 possible evolutionarily accessible trajectories of A2F.Two levels of Δλmax (<25 or > 25 nm) are shown by black and red lines, respectively. A251643F (in black) is compared to those with pure epistatic interactions among TM I–VII (in blue) and TM I–III (in blue broken line).
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