Can the Dynamic Colouration and Patterning of Bluelined Goatfish (Mullidae; Upeneichthys lineatus) Be Perceived by Conspecifics?

Bluelined goatfish (<i>Upeneichthys lineatus</i>) exhibit dynamic body colour changes and transform rapidly from a pale, buff/white, horizontally banded pattern to a conspicuous, vertically striped, red pattern when foraging. This red pattern is potentially an important foraging signal for communication with conspecifics, provided that <i>U. lineatus</i> can detect and discriminate the pattern. Using both physiological and behavioural experiments, we first examined whether <i>U. lineatus</i> possess visual pigments with sensitivity to long (“red”) wavelengths of light, and whether they can discriminate the colour red. Microspectrophotometric measurements of retinal photoreceptors showed that while <i>U. lineatus</i>lack visual pigments dedicated to the red part of the spectrum, their pigments likely confer some sensitivity in this spectral band. Behavioural colour discrimination experiments suggested that <i>U. lineatus</i>can distinguish a red reward stimulus from a grey distractor stimulus of variable brightness. Furthermore, when presented with red stimuli of varying brightness they could mostly discriminate the darker and lighter reds from the grey distractor. We also obtained anatomical estimates of visual acuity, which suggest that <i>U. lineatus</i> can resolve the contrasting bands of conspecifics approximately 7 m away in clear waters. Finally, we measured the spectral reflectance of the red and white colouration on the goatfish body. Visual models suggest that <i>U. lineatus</i> can discriminate both chromatic and achromatic differences in body colouration where longer wavelength light is available. This study demonstrates that <i>U. lineatus</i> have the capacity for colour vision and can likely discriminate colours in the long-wavelength region of the spectrum where the red body pattern reflects light strongly. The ability to see red may therefore provide an advantage in recognising visual signals from conspecifics. This research furthers our understanding of how visual signals have co-evolved with visual abilities, and the role of visual communication in the marine environment.

Evolutionary analyses of visual opsin genes in anurans reveals diversity and positive selection suggestive of functional adaptation to distinct light environments

Among major vertebrate groups, anurans (frogs and toads) are understudied with regards to their visual systems and little is known about variation among species that differ in ecology. We sampled North American anurans representing diverse evolutionary and life histories that likely possess visual systems adapted to meet different ecological needs. Using standard molecular techniques, visual opsin genes, which encode the protein component of visual pigments, were obtained from anuran retinas. Additionally, we extracted the visual opsins from publicly available genome and transcriptome assemblies, further increasing the phylogenetic and ecological diversity of our dataset. We found that anurans consistently express four visual opsin genes (RH1, LWS, SWS1, and SWS2, but not RH2) even though reported photoreceptor complements vary widely among species. We found the first evidence of visual opsin duplication in an amphibian with the duplication of the LWS gene in the African bullfrog, which had distinct LWS copies on the sex chromosomes. The proteins encoded by these genes showed considerable sequence variation among species, including at sites known to shift the spectral sensitivity of visual pigments in other vertebrates and thus mediate dim-light and color vision. Using molecular evolutionary analyses of selection (dN/dS) we found significant evidence for positive selection at a subset of sites in the dim-light rod opsin gene RH1 and the long wavelength sensitive cone opsin gene LWS. The function of sites inferred to be under positive selection are largely unknown, but a few are likely to affect spectral sensitivity and other visual pigment functions based on proximity to previously identified sites in other vertebrates. The observed variation cannot fully be explained by evolutionary relationships among species alone. Taken together, our results suggest that other ecological factors, such as habitat and life history, as well as behaviour, may be driving changes to anuran visual systems.

The diversity of opsins in Lake Baikal amphipods (Amphipoda: Gammaridae)

Background Vision is a crucial sense for the evolutionary success of many animal groups. Here we explore the diversity of visual pigments (opsins) in the transcriptomes of amphipods (Crustacea: Amphipoda) and conclude that it is restricted to middle (MWS) and long wavelength-sensitive (LWS) opsins in the overwhelming majority of examined species. Results We evidenced (i) parallel loss of MWS opsin expression in multiple species (including two independently evolved lineages from the deep and ancient Lake Baikal) and (ii) LWS opsin amplification (up to five transcripts) in both Baikal lineages. The number of LWS opsins negatively correlated with habitat depth in Baikal amphipods. Some LWS opsins in Baikal amphipods contained MWS-like substitutions, suggesting that they might have undergone spectral tuning. Conclusions This repeating two-step evolutionary scenario suggests common triggers, possibly the lack of light during the periods when Baikal was permanently covered with thick ice and its subsequent melting. Overall, this observation demonstrates the possibility of revealing climate history by following the evolutionary changes in protein families.

Shedding new light on the generation of the visual chromophore

The visual phototransduction cascade begins with acis–transphotoisomerization of a retinylidene chromophore associated with the visual pigments of rod and cone photoreceptors. Visual opsins release their all-trans-retinal chromophore following photoactivation, which necessitates the existence of pathways that produce 11-cis-retinal for continued formation of visual pigments and sustained vision. Proteins in the retinal pigment epithelium (RPE), a cell layer adjacent to the photoreceptor outer segments, form the well-established “dark” regeneration pathway known as the classical visual cycle. This pathway is sufficient to maintain continuous rod function and support cone photoreceptors as well although its throughput has to be augmented by additional mechanism(s) to maintain pigment levels in the face of high rates of photon capture. Recent studies indicate that the classical visual cycle works together with light-dependent processes in both the RPE and neural retina to ensure adequate 11-cis-retinal production under natural illuminances that can span ten orders of magnitude. Further elucidation of the interplay between these complementary systems is fundamental to understanding how cone-mediated vision is sustained in vivo. Here, we describe recent advances in understanding how 11-cis-retinal is synthesized via light-dependent mechanisms.

Light-induced difference FTIR spectroscopy of primate blue-sensitive visual pigment at 163 K

ABSTRACTStructural studies of color visual pigments lag far behind those of rhodopsin for scotopic vision. Using difference FTIR spectroscopy at 77 K, we report the first structural data of three primate color visual pigments, monkey red (MR), green (MG), and blue (MB), where the batho-intermediate (Batho) exhibits photoequilibrium with the unphotolyzed state. This photochromic property is highly advantageous for limited samples since the signal-to-noise ratio is improved, but may not be applicable to late intermediates, because of large structural changes to proteins. Here we report the photochromic property of MB at 163 K, where the BL intermediate, formed by the relaxation of Batho, is in photoequilibrium with the initial MB state. A comparison of the difference FTIR spectra at 77 and 163 K provided information on what happens in the process of transition from Batho to BL in MB. The coupled C11=C12 HOOP vibration in the planer structure in MB is decoupled by distortion in Batho after retinal photoisomerization, but returns to the coupled C11=C12 HOOP vibration in the all-trans chromophore in BL. This suggests that BL harbors a planer all-trans configuration of retinal. The Batho formation accompanies helical structural perturbation, which is relaxed in BL. The H-D unexchangeable X-H stretch weakens the hydrogen bond in Batho, but strengthens it in BL. Protein-bound water molecules that form an extended water cluster near the retinal chromophore change hydrogen bonds differently for Batho and BL, being stronger in the latter than in the initial state. In addition to structural dynamics, the present FTIR spectra at 163 K show no signals of protonated carboxylic acids as well as 77 K, suggesting that E181 is deprotonated in MB, Batho and BL.

Unique retinal binding pocket of primate blue-sensitive visual pigment

ABSTRACTThe visual pigments of humans contain 11-cis retinal as the chromophore of light perception, and its photoisomerization to the all-trans form initiates visual excitation in our eyes. It is well known that three isomeric states of retinal (11-cis, all-trans, and 9-cis) are in photoequilibrium at very low temperatures such as 77 K. Here we report the lack of formation of the 9-cis form in monkey blue (MB) at 77 K, as revealed by light-induced difference FTIR spectroscopy. This indicates that the chromophore binding pocket of MB does not accommodate the 9-cis form, even though it accommodates the all-trans form by twisting the chromophore. Mutation of the blue-specific tyrosine at position 265 into tryptophan, which is highly conserved in other animal rhodopsins, led to formation of the 9-cis form in MB, suggesting that Y265 is one of the determinants of the unique photochemistry in blue pigments. We also found that 9-cis retinal does not bind to MB opsin, implying that the chromophore binding pocket does not accommodate the 9-cis form at physiological temperature. The unique property of MB is discussed based on the present results.

Exceptional diversity of opsin expression patterns in Neogonodactylus oerstedii (Stomatopoda) retinas

Stomatopod crustaceans possess some of the most complex animal visual systems, including at least 16 spectrally distinct types of photoreceptive units (e.g., assemblages of photoreceptor cells). Here we fully characterize the set of opsin genes expressed in retinal tissues and determine expression patterns of each in the stomatopod Neogonodactylus oerstedii. Using a combination of transcriptome and RACE sequencing, we identified 33 opsin transcripts expressed in each N. oerstedii eye, which are predicted to form 20 long-wavelength–sensitive, 10 middle-wavelength–sensitive, and three UV-sensitive visual pigments. Observed expression patterns of these 33 transcripts were highly unusual in five respects: 1) All long-wavelength and short/middle-wavelength photoreceptive units expressed multiple opsins, while UV photoreceptor cells expressed single opsins; 2) most of the long-wavelength photoreceptive units expressed at least one middle-wavelength–sensitive opsin transcript; 3) the photoreceptors involved in spatial, motion, and polarization vision expressed more transcripts than those involved in color vision; 4) there is a unique opsin transcript that is expressed in all eight of the photoreceptive units devoted to color vision; and 5) expression patterns in the peripheral hemispheres of the eyes suggest visual specializations not previously recognized in stomatopods. Elucidating the expression patterns of all opsin transcripts expressed in the N. oerstedii retina reveals the potential for previously undocumented functional diversity in the already complex stomatopod eye and is a first step toward understanding the functional significance of the unusual abundance of opsins found in many arthropod species’ visual systems.