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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 - Sci Adv (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Emory University, Atlanta, GA 30322, USA.

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.

No MeSH data available.


Related in: MedlinePlus

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.)
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Figure 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.)

Mentions: We inferred the 12 amino acids present at the nodes of a phylogenetic tree during the frog-423 evolution by using 14 representative pigments (fig. S2) and the maximum likelihood–based Bayesian method [phylogenetic analysis by maximum likelihood (PAML) (35) with Jones-Taylor-Thornton (JTT) and Whelan and Goldman (WAG) substitution models]. In particular, we inferred the amino acids at the 12 sites of three ancestral pigments in a composite tree of 14 representative SWS1 pigments: (i) AncAmphibian-359; (ii) the common ancestor of African clawed frog, Western clawed frog, and bullfrog pigments (AncFrog); and (iii) the common ancestor of the two clawed frog pigments (AncClawed-frog) (fig. S2). The 12 amino acids predicted using the two models have very similar PPs and are highly consistent (table S1). With the exception of site 109, the amino acids of AncAmphibian-359 have a PP of >0.95 and are highly reliable. For AncClawed-frog, all 12 amino acids have a PP of >0.90. For AncFrog, the amino acids (sites 113 to 277) in TM III–VI are more reliable than those (sites 49 to 93) in TM I-II. When the frog-423 evolution is divided into three stages, that is, from AncAmphibian-359 to AncFrog (stage 1), from AncFrog to AncClawed-frog (stage 2), and from AncClawed-frog to frog-423 (stage 3), most of the adaptive changes occurred in stages 1 and 2 (Fig. 3), in which the levels of reliabilities of the 12 inferred amino acids using the JTT model are also indicated using the logos.


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 - Sci Adv (2015)

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.)
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4643761&req=5

Figure 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.)
Mentions: We inferred the 12 amino acids present at the nodes of a phylogenetic tree during the frog-423 evolution by using 14 representative pigments (fig. S2) and the maximum likelihood–based Bayesian method [phylogenetic analysis by maximum likelihood (PAML) (35) with Jones-Taylor-Thornton (JTT) and Whelan and Goldman (WAG) substitution models]. In particular, we inferred the amino acids at the 12 sites of three ancestral pigments in a composite tree of 14 representative SWS1 pigments: (i) AncAmphibian-359; (ii) the common ancestor of African clawed frog, Western clawed frog, and bullfrog pigments (AncFrog); and (iii) the common ancestor of the two clawed frog pigments (AncClawed-frog) (fig. S2). The 12 amino acids predicted using the two models have very similar PPs and are highly consistent (table S1). With the exception of site 109, the amino acids of AncAmphibian-359 have a PP of >0.95 and are highly reliable. For AncClawed-frog, all 12 amino acids have a PP of >0.90. For AncFrog, the amino acids (sites 113 to 277) in TM III–VI are more reliable than those (sites 49 to 93) in TM I-II. When the frog-423 evolution is divided into three stages, that is, from AncAmphibian-359 to AncFrog (stage 1), from AncFrog to AncClawed-frog (stage 2), and from AncClawed-frog to frog-423 (stage 3), most of the adaptive changes occurred in stages 1 and 2 (Fig. 3), in which the levels of reliabilities of the 12 inferred amino acids using the JTT model are also indicated using the logos.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Emory University, Atlanta, GA 30322, USA.

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.

No MeSH data available.


Related in: MedlinePlus