Abstract

BackgroundMany vertebrate species use ultraviolet (UV) reception for such basic behaviors as foraging and mating, but many others switched to violet reception and improved their visual resolution. The respective phenotypes are regulated by the short wavelength-sensitive (SWS1) pigments that absorb light maximally (λmax) at ~360 and 395–440 nm. Because of strong epistatic interactions, the biological significance of the extensive mutagenesis results on the molecular basis of spectral tuning in SWS1 pigments and the mechanisms of their phenotypic adaptations remains uncertain.ResultsThe magnitudes of the λmax-shifts caused by mutations in a present-day SWS1 pigment and by the corresponding forward mutations in its ancestral pigment are often dramatically different. To resolve these mutagenesis results, the A/B ratio, in which A and B are the areas formed by amino acids at sites 90, 113 and 118 and by those at sites 86, 90 and 118 and 295, respectively, becomes indispensable. Then, all critical mutations that generated the λmax of a SWS1 pigment can be identified by establishing that 1) the difference between the λmax of the ancestral pigment with these mutations and that of the present-day pigment is small (3 ~ 5 nm, depending on the entire λmax-shift) and 2) the difference between the corresponding A/B ratios is < 0.002.ConclusionMolecular adaptation has been studied mostly by using comparative sequence analyses. These statistical results provide biological hypotheses and need to be tested using experimental means. This is an opportune time to explore the currently available and new genetic systems and test these statistical hypotheses. Evaluating the λmaxs and A/B ratios of mutagenized present-day and their ancestral pigments, we now have a method to identify all critical mutations that are responsible for phenotypic adaptation of SWS1 pigments. The result also explains spectral tuning of the same pigments, a central unanswered question in phototransduction.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0637-9) contains supplementary material, which is available to authorized users.

Highlights

  • Many vertebrate species use ultraviolet (UV) reception for such basic behaviors as foraging and mating, but many others switched to violet reception and improved their visual resolution

  • To recapitulate the evolution of a certain present-day pigment, molecular evolutionists infer the evolution in a reverse fashion by introducing mutations into the present-day pigment, but the magnitudes of λmax-shift caused by these mutations and the corresponding forward mutations in its ancestral pigment can differ drastically [11,12,13, 16, 17]

  • Since JTT and WAG models predict very similar ancestral sequences, we used the amino acid sequences predicted by JTT model (Additional file 2: Figure S1) and introduced the necessary amino acid changes into the internal segment in the pMT5 containing the N- and C-termini of the chameleon-359 and engineered AncVertebrate, AncTetrapod, AncAmphibian, AncAmniote as well as those of Euteleosts (AncEuteleost), Mammals (AncMammal) and Eutherians (AncEutheria) (Additional file 2: Figure S1; Fig. 1a)

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Summary

Introduction

Many vertebrate species use ultraviolet (UV) reception for such basic behaviors as foraging and mating, but many others switched to violet reception and improved their visual resolution. UV and violet reception are regulated by the short wavelength-sensitive (SWS1) pigments that absorb light maximally (λmax) at ~360 and 395–440 nm, respectively [1]. Using the traditional experimental approach, multiple sets of mutations can explain an observed λmax and the evolutionary mechanisms inferred can be misleading or even erroneous [14, 15, 18, 19]. This “multiple-solution” problem occurs because 1) pigment-specific non-additive (epistatic) interactions are ignored and 2) the current mutagenesis experiments are used to search for “any” mutations that can achieve targeted λmaxs.

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