The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies

Liénard, Marjorie A.; Bernard, Gary D.; Allen, Andrew; Lassance, Jean-Marc; Song, Siliang; Childers, Richard Rabideau; Yu, Nanfang; Ye, Dajia; Stephenson, Adriana; Valencia-Montoya, Wendy A; Salzman, Shayla; Whitaker, Melissa R. L.; Calonje, Michael; Zhang, Feng; Pierce, Naomi E.

doi:10.1073/pnas.2008986118

Cited by 41 publications

(58 citation statements)

References 156 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The telltale sign for the presence of G+R− cells are red-shining ommatidia. A similar implementation of the red colour channel might exist in Lycaenidae [ 24 ], while in Pieridae and Papilionidae, R5–8 have assumed the role of red receptors instead [ 1 ], and the role of R9 in these two families is not known. The red channel appears to be absent from nymphalid butterflies with uniform eyeshine.…”

Section: Discussionmentioning

confidence: 99%

Red-green opponency in the long visual fibre photoreceptors of brushfoot butterflies (Nymphalidae)

et al. 2021

View full text Add to dashboard Cite

In many butterflies, the ancestral trichromatic insect colour vision, based on UV-, blue- and green-sensitive photoreceptors, is extended with red-sensitive cells. Physiological evidence for red receptors has been missing in nymphalid butterflies, although some species can discriminate red hues well. In eight species from genera Archaeoprepona, Argynnis, Charaxes, Danaus, Melitaea, Morpho, Heliconius and Speyeria , we found a novel class of green-sensitive photoreceptors that have hyperpolarizing responses to stimulation with red light. These green-positive, red-negative (G+R–) cells are allocated to positions R1/2, normally occupied by UV and blue-sensitive cells. Spectral sensitivity, polarization sensitivity and temporal dynamics suggest that the red opponent units (R–) are the basal photoreceptors R9, interacting with R1/2 in the same ommatidia via direct inhibitory synapses. We found the G+R– cells exclusively in butterflies with red-shining ommatidia, which contain longitudinal screening pigments. The implementation of the red colour channel with R9 is different from pierid and papilionid butterflies, where cells R5–8 are the red receptors. The nymphalid red-green opponent channel and the potential for tetrachromacy seem to have been switched on several times during evolution, balancing between the cost of neural processing and the value of extended colour information.

show abstract

Section: Discussionmentioning

confidence: 99%

Red-green opponency in the long visual fibre photoreceptors of brushfoot butterflies (Nymphalidae)

et al. 2021

View full text Add to dashboard Cite

show abstract

“…570 nm 48 – 51 . In most insects with peak sensitivities beyond 570 nm, the shift to longer sensitivity is achieved through red or orange pigments which act as filters 11 , 44 , 52 , 53 (but see Papilio and Eumaeus that shift through opsin sequence modification 21 , 22 ). Therefore, we generated LWS spectral sensitivity curves by applying cut-off filters to the 570 nm A1-based profile (Fig.…”

Section: Methodsmentioning

confidence: 99%

Insect visual sensitivity to long wavelengths enhances colour contrast of insects against vegetation

Wang

Stuart‐Fox

Walker

et al. 2022

Sci Rep

View full text Add to dashboard Cite

The sensitivity of animal photoreceptors to different wavelengths of light strongly influence the perceived visual contrast of objects in the environment. Outside of the human visual wavelength range, ultraviolet sensitivity in many species provides important and behaviourally relevant visual contrast between objects. However, at the opposite end of the spectrum, the potential advantage of red sensitivity remains unclear. We investigated the potential benefit of long wavelength sensitivity by modelling the visual contrast of a wide range of jewel beetle colours against flowers and leaves of their host plants to hypothetical insect visual systems. We find that the presence of a long wavelength sensitive photoreceptor increases estimated colour contrast, particularly of beetles against leaves. Moreover, under our model parameters, a trichromatic visual system with ultraviolet (λmax = 355 nm), short (λmax = 445 nm) and long (λmax = 600 nm) wavelength photoreceptors performed as well as a tetrachromatic visual system, which had an additional medium wavelength photoreceptor (λmax = 530 nm). When we varied λmax for the long wavelength sensitive receptor in a tetrachromatic system, contrast values between beetles, flowers and leaves were all enhanced with increasing λmax from 580 nm to at least 640 nm. These results suggest a potential advantage of red sensitivity in visual discrimination of insect colours against vegetation and highlight the potential adaptive value of long wavelength sensitivity in insects.

show abstract

“…The rhodopsin proteorhodopsin and related proteins have aroused continuous and extensive interest both experimentally and theoretically among researchers, especially during the past 20 years [ 1 , 2 , 3 , 4 , 5 ]. Rhodopsin is a seven transmembrane α-helices (TM) protein which uses retinal as a chromophore.…”

Section: Introductionmentioning

confidence: 99%

Accurate Prediction of Absorption Spectral Shifts of Proteorhodopsin Using a Fragment-Based Quantum Mechanical Method

et al. 2021

View full text Add to dashboard Cite

Many experiments have been carried out to display different colors of Proteorhodopsin (PR) and its mutants, but the mechanism of color tuning of PR was not fully elucidated. In this study, we applied the Electrostatically Embedded Generalized Molecular Fractionation with Conjugate Caps (EE-GMFCC) method to the prediction of excitation energies of PRs. Excitation energies of 10 variants of Blue Proteorhodopsin (BPR-PR105Q) in residue 105GLN were calculated with the EE-GMFCC method at the TD-B3LYP/6-31G* level. The calculated results show good correlation with the experimental values of absorption wavelengths, although the experimental wavelength range among these systems is less than 50 nm. The ensemble-averaged electric fields along the polyene chain of retinal correlated well with EE-GMFCC calculated excitation energies for these 10 PRs, suggesting that electrostatic interactions from nearby residues are responsible for the color tuning. We also utilized the GMFCC method to decompose the excitation energy contribution per residue surrounding the chromophore. Our results show that residues ASP97 and ASP227 have the largest contribution to the absorption spectral shift of PR among the nearby residues of retinal. This work demonstrates that the EE-GMFCC method can be applied to accurately predict the absorption spectral shifts for biomacromolecules.

show abstract

The evolution of red color vision is linked to coordinated rhodopsin tuning in lycaenid butterflies

Cited by 41 publications

References 156 publications

Red-green opponency in the long visual fibre photoreceptors of brushfoot butterflies (Nymphalidae)

Red-green opponency in the long visual fibre photoreceptors of brushfoot butterflies (Nymphalidae)

Insect visual sensitivity to long wavelengths enhances colour contrast of insects against vegetation

Accurate Prediction of Absorption Spectral Shifts of Proteorhodopsin Using a Fragment-Based Quantum Mechanical Method

Contact Info

Product

Resources

About