scholarly journals Opsin gene evolution in amphibious and terrestrial combtooth blennies (Blenniidae)

2018 ◽  
Author(s):  
Fabio Cortesi ◽  
Karen M Cheney ◽  
Georgina M Cooke ◽  
Terry Ord

Evolutionary adaptations to life on land include changes to the physiology, morphology and behaviour of an animal in response to physical differences between water and air. The visual systems of amphibious species show pronounced morphological adaptations; yet, whether molecular changes also occur remains largely unknown. Here, we investigated the molecular evolution of visual pigment genes (opsins) in amphibious and terrestrial fishes belonging to the Salariini division of blennies (Blenniidae). We hypothesized that when conquering land, blenny opsins adapt, in terms of sequence variation and/or gene expression, to match both higher light intensities as well as the broader light spectrum. Using retinal transcriptomes in six species ranging from fully aquatic to fully terrestrial, we found very little variation in opsin gene sequences or gene expression between species. All blennies expressed a single rod opsin gene as well as two cone opsin genes sensitive to longer-wavelengths of light: RH2A-1 (green-sensitive) and LWS (red-sensitive). They also expressed one or two short-wavelength-sensitive cone opsin genes (SWS2Aα, SWS2Aβ; blue-sensitive) in a phylogenetically inert manner. However, based on amino acid predictions, both SWS2A proteins confer similar peak spectral sensitivities and differential expression is therefore unlikely to be ecologically significant. Red-sensitivity is likely beneficial for feeding on algae and detritus, the main food source of Salariini blennies, and could be co-adapted to perceive visual displays in terrestrial species, which often use red dorsal fins to signal during aggressive disputes and courtship. Our data suggests that on the molecular level, the visual systems that evolved in aquatic blennies have been retained in species that have transitioned onto land.

2019 ◽  
Vol 116 (10) ◽  
pp. 4651-4660 ◽  
Author(s):  
Yohey Ogawa ◽  
Tomoya Shiraki ◽  
Yoshimasa Asano ◽  
Akira Muto ◽  
Koichi Kawakami ◽  
...  

Color discrimination in the vertebrate retina is mediated by a combination of spectrally distinct cone photoreceptors, each expressing one of multiple cone opsins. The opsin genes diverged early in vertebrate evolution into four classes maximally sensitive to varying wavelengths of light: UV (SWS1), blue (SWS2), green (RH2), and red (LWS) opsins. Although the tetrachromatic cone system is retained in most nonmammalian vertebrate lineages, the transcriptional mechanism underlying gene expression of the cone opsins remains elusive, particularly for SWS2 and RH2 opsins, both of which have been lost in the mammalian lineage. In zebrafish, which have all four cone subtypes,rh2opsin gene expression depends on a homeobox transcription factor,sine oculishomeobox 7 (Six7). However, thesix7gene is found only in the ray-finned fish lineage, suggesting the existence of another evolutionarily conserved transcriptional factor(s) controllingrh2opsin expression in vertebrates. Here, we found that the reducedrh2expression caused bysix7deficiency was rescued by forced expression ofsix6b, which is asix7-related transcription factor conserved widely among vertebrates. The compensatory role ofsix6bwas reinforced by ChIP-sequencing analysis, which revealed a similar pattern of Six6b- and Six7-binding sites within and near the cone opsin genes. TAL effector nuclease-induced genetic ablation ofsix6bandsix7revealed that they coordinately regulate SWS2 opsin gene expression. Mutant larvae deficient for these transcription factors showed severely impaired visually driven foraging behavior. These results demonstrate that in zebrafish,six6bandsix7govern expression of the SWS2 and RH2 opsins responsible for middle-wavelength sensitivity, which would be physiologically important for daylight vision.


2019 ◽  
Author(s):  
Martin Luehrmann ◽  
Fabio Cortesi ◽  
Karen L. Cheney ◽  
Fanny de Busserolles ◽  
N. Justin Marshall

AbstractVertebrates exhibit diverse visual systems that vary in terms of morphology, number and distribution of spectrally distinct photoreceptor types, visual opsin genes and gene expression levels.In fish, such adaptations are driven by two main factors: differences in the light environment and behavioural tasks, including foraging, predator avoidance and mate selection. Whether visual systems also adapt to small-scale spectral differences in light, between microhabitats, is less clear.We suggest that differences in microhabitat use by cardinalfishes (Apogonidae) on coral reefs drive morphological and molecular adaptations in their visual systems. To test this, we investigated diurnal microhabitat use in 17 cardinalfish species and assessed whether this correlated with differences in visual opsin gene expression and eye morphology.We found that cardinalfishes display six types of partitioning behaviours during the day, ranging from specialists found exclusively in the water column to species that are always hidden inside the reef matrix.Using data on visual opsin gene expression previously characterized in this family, it was discovered that species in exposed habitats had increased expression of the short-wavelength sensitive violet opsin (SWS2B) and decreased expression of the dim-light active rod opsin (RH1). Species of intermediate exposure, on the other hand, expressed opsins that are mostly sensitive to the blue-green central part of the light spectrum (SWS2As and RH2s), while fishes entirely hidden in the reef substrate had an increased expression of the long-wavelength sensitive red opsin (LWS).We found that eye size relative to body size significantly differed between cardinalfish species, and relative eye size decreased with an increase in habitat exposure.Retinal topography did not show co-adaptation with microhabitat use, but instead with feeding mode.We suggest that, although most cardinalfishes are nocturnal foragers, their visual systems are also adapted to both the light intensity and the light spectrum of their preferred diurnal microhabitat.


1999 ◽  
Vol 16 (3) ◽  
pp. 601-605 ◽  
Author(s):  
ELLEN A. SCHMITT ◽  
GEORGE A. HYATT ◽  
JOHN E. DOWLING

We report here a reexamination of the developmental expression of cone opsins in the zebrafish retina. The red- and blue-sensitive opsins appear at 51 h postfertilization (hpf) whereas ultraviolet (UV) opsin is not seen until after 55 hpf. More cells show red cone opsin expression than blue at 51 and 55 hpf, indicating the sequence of cone opsin expression in zebrafish is first red, then blue, and finally UV. Curiously, morphological development of the cones is in reverse order; UV cones appear quite mature by day 6–7 postfertilization (pf), but morphologically, red cones do not appear adult-like until 15–20 days pf.


2006 ◽  
Vol 23 (3-4) ◽  
pp. 379-385 ◽  
Author(s):  
MAUREEN NEITZ ◽  
SHAWN D. BALDING ◽  
CARRIE MCMAHON ◽  
STACY A. SJOBERG ◽  
JAY NEITZ

The topographical distributions of the relative ratio of long- (L) and middle- (M) wavelength sensitive cone opsin messenger RNA (mRNA) in human and baboon retinas were mapped using real-time polymerase chain reaction. The L:M mRNA ratio increased in a central-to-peripheral gradient in both species, being quite pronounced for humans.


2015 ◽  
Vol 282 (1798) ◽  
pp. 20142321 ◽  
Author(s):  
Natasha I. Bloch

Theories of sexual and natural selection predict coevolution of visual perception with conspecific colour and/or the light environment animals occupy. One way to test these theories is to focus on the visual system, which can be achieved by studying the opsin-based visual pigments that mediate vision. Birds vary greatly in colour, but opsin gene coding sequences and associated visual pigment spectral sensitivities are known to be rather invariant across birds. Here, I studied expression of the four cone opsin genes ( Lws, Rh2, Sws2 and Sws1 ) in 16 species of New World warblers (Parulidae). I found levels of opsin expression vary both across species and between the sexes. Across species, female, but not male Sws2 expression is associated with an index of sexual selection, plumage dichromatism. This fits predictions of classic sexual selection models, in which the sensory system changes in females, presumably impacting female preference, and co-evolves with male plumage. Expression of the opsins at the extremes of the light spectrum, Lws and Uvs, correlates with the inferred light environment occupied by the different species. Unlike opsin spectral tuning, regulation of opsin gene expression allows for fast adaptive evolution of the visual system in response to natural and sexual selection, and in particular, sex-specific selection pressures.


2016 ◽  
Vol 88 (3-4) ◽  
pp. 204-212 ◽  
Author(s):  
Da-Wei Liu ◽  
Ying Lu ◽  
Hong Young Yan ◽  
Harold H. Zakon

Losses of cone opsin genes are noted in animals that are nocturnal or rely on senses other than vision. We investigated the cone opsin repertoire of night-active South American weakly electric fish. We obtained opsin gene sequences from genomic DNA of 3 gymnotiforms (Eigenmannia virescens, Sternopygus macrurus, Apteronotus albifrons) and the assembled genome of the electric eel (Electrophorus electricus). We identified genes for long-wavelength-sensitive (LWS) and medium-wavelength-sensitive cone opsins (RH2) and rod opsins (RH1). Neither of the 2 short-wavelength-sensitive cone opsin genes were found and are presumed lost. The fact that Electrophorus has a complete repertoire of extraretinal opsin genes and conservation of synteny with the zebrafish (Danio rerio) for genes flanking the 2 short-wavelength-sensitive opsin genes supports the supposition of gene loss. With microspectrophotometry and electroretinograms we observed absorption spectra consistent with RH1 and LWS but not RH2 opsins in the retinal photoreceptors of E. virescens. This profile of opsin genes and their retinal expression is identical to the gymnotiform's sister group, the catfish, which are also nocturnally active and bear ampullary electroreceptors, suggesting that this pattern likely occurred in the common ancestor of gymnotiforms and catfish. Finally, we noted an unusual N-terminal motif lacking a conserved glycosylation consensus site in the RH2 opsin of gymnotiforms, a catfish and a characin (Astyanax mexicanus). Mutations at this site influence rhodopsin trafficking in mammalian photoreceptors and cause retinitis pigmentosa. We speculate that this unusual N terminus may be related to the absence of the RH2 opsin in the cones of gymnotiforms and catfish.


2020 ◽  
Author(s):  
Nik Lupše ◽  
Fabio Cortesi ◽  
Marko Freese ◽  
Lasse Marohn ◽  
Jan-Dag Pohlman ◽  
...  

AbstractDeep-sea fishes show extraordinary visual adaptations to an environment where every photon of light that is captured might make the difference between life and death. While considerable effort has been made in understanding how adult deep-sea fishes see their world, relatively little is known about vision in earlier life stages. Similar to most marine species, larval deep-sea fishes start their life in the well-lit epipelagic zone, where food is abundant and predation relatively low. In this study, we show major changes in visual gene expression between larval and adult deep-sea fishes from eight different orders (Argentiniformes, Aulopiformes, Beryciformes, Myctophiformes, Pempheriformes, Scombriformes, Stomiiformes and Trachichthyiformes). Comparison between 18 species revealed that while adults mostly rely on rod opsin(s) (RH1) for vision in dim-light, larvae mostly express green-sensitive cone opsin(s) (RH2) in their retinas. Adults of the scombriform and three aulopiform species also expressed low levels of RH2, with the latter using different copies of the gene between ontogenetic stages. Cone opsins in adult fishes are rather surprising as most deep-sea fishes have lost their cone photoreceptors in favour of a highly sensitive pure rod retina. The expression of RH2 in larvae, on the other hand, shows that even in species that might not have any cones as adults, the larval retina is likely to be cone dominated first, before rod photoreceptors are added through ontogeny. Our study therefore supports a conserved pathway for the cone-to-rod developmental sequence of the teleost or even vertebrate retina.


2021 ◽  
Author(s):  
Yohey Ogawa ◽  
Tomoya Shiraki ◽  
Yoshitaka Fukada ◽  
Daisuke Kojima

In vertebrates, daylight vision is mediated by a combination of spectrally distinct cone photoreceptor cells. Most vertebrate lineages retain a tetrachromatic cone system in which each cone photoreceptor subtype expresses one of four cone opsins: UV- (SWS1), blue- (SWS2), green- (RH2), and red-sensitive (LWS) opsins. Each cone subtype identity is established by a transcriptional network directing selective opsin gene expression in single photoreceptors. Our knowledge is limited regarding gene expression mechanisms for the middle wavelength-sensitive opsin genes, sws2 and rh2, because they are absent in mammalian species such as mouse, whose visual system has been extensively studied. Our previous studies identified homeobox transcription factors, Six6 and Six7, as crucial regulators of both sws2 and rh2 gene expression in zebrafish. Yet it remains unclear how these two opsin genes are selectively expressed in a cone subtype-specific manner. Here we pursued loss-of-function studies on transcription factors expressed predominantly in zebrafish cone photoreceptors and found that sws2 expression requires a forkhead box transcription factor, Foxq2, which is retained in many vertebrates having sws2 gene. A quantitative gene expression analysis using purified pools of the four cone subtypes revealed that foxq2 was expressed only in SWS2 cone subtype. foxq2 expression was abrogated in six6a/six6b/six7 knock-out zebrafish, which is deficient in SWS2 cone subtype. Forced expression of foxq2 fully restored sws2 expression in six7 knock-out fish without affecting rh2 expression. We propose a core transcriptional network that determines SWS2 cone subtype identity in the tetrachromatic vertebrate.


2021 ◽  
Author(s):  
Ryan K Schott ◽  
Leah Perez ◽  
Matthew A Kwiatkowski ◽  
Vance Imhoff ◽  
Jennifer M Gumm

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.


Sign in / Sign up

Export Citation Format

Share Document