Single-gene and whole-genome duplications are important evolutionary mechanisms that contribute to biological diversification by launching new genetic raw material. For example, the evolution of ...animal vision is tightly linked to the expansion of the opsin gene family encoding light-absorbing visual pigments. In teleost fishes, the most species-rich vertebrate group, opsins are particularly diverse and key to the successful colonization of habitats ranging from the bioluminescence-biased but basically dark deep sea to clear mountain streams. In this study, we report a previously unnoticed duplication of the violet-blue short wavelength-sensitive 2 (SWS2) opsin, which coincides with the radiation of highly diverse percomorph fishes, permitting us to reinterpret the evolution of this gene family. The inspection of close to 100 fish genomes revealed that, triggered by frequent gene conversion between duplicates, the evolutionary history of SWS2 is rather complex and difficult to predict. Coincidentally, we also report potential cases of gene resurrection in vertebrate opsins, whereby pseudogenized genes were found to convert with their functional paralogs. We then identify multiple novel amino acid substitutions that are likely to have contributed to the adaptive differentiation between SWS2 copies. Finally, using the dusky dottyback Pseudochromis fuscus , we show that the newly discovered SWS2A duplicates can contribute to visual adaptation in two ways: by gaining sensitivities to different wavelengths of light and by being differentially expressed between ontogenetic stages. Thus, our study highlights the importance of comparative approaches in gaining a comprehensive view of the dynamics underlying gene family evolution and ultimately, animal diversification.
Significance Gene and whole-genome duplications are important evolutionary forces promoting organismal diversification. Teleost fishes, for example, possess many gene duplicates responsible for photoreception (opsins), which emerged through gene duplication and allow fishes to adapt to the various light conditions of the aquatic environment. Here, we reevaluate the evolutionary history of the violet-blue–sensitive opsins short wavelength-sensitive 2 (SWS2) in modern teleosts using next generation genome sequencing. We uncover a gene duplication event specific to the most diverse lineage of vertebrates (the percomorphs) and show that SWS2 evolution was highly dynamic and involved gene loss, pseudogenization, and gene conversion. We, thus, clarify previous discrepancies regarding opsin annotations. Our study highlights the importance of integrative approaches to help us understand how species adapt and diversify.
Colour vision in marine organisms Marshall, Justin; Carleton, Karen L; Cronin, Thomas
Current opinion in neurobiology,
10/2015, Volume:
34
Journal Article
Peer reviewed
Highlights • Most marine animals possess no or relatively simple colour vision, for example, monochromacy or dichromacy. • The 12 spectral channel unconventional colour vision of stomatopods is an ...exception in the ocean. • Colour vision diversity is greater in the ocean than on land due to extremes in photic habitat and colour behaviours. • Sequencing may reveal more opsins than functional at any one time, but which provide substrate for rapid adaptation. • There is an as yet unexplained diversity of colour vision and colour signals among teleost fish possibly resulting from neutral drift.
Among vertebrates, teleost eye diversity exceeds that found in all other groups. Their spectral sensitivities range from ultraviolet to red, and the number of visual pigments varies from 1 to over ...40. This variation is correlated with the different ecologies and life histories of fish species, including their variable aquatic habitats: murky lakes, clear oceans, deep seas and turbulent rivers. These ecotopes often change with the season, but fish may also migrate between ecotopes diurnally, seasonally or ontogenetically. To survive in these variable light habitats, fish visual systems have evolved a suite of mechanisms that modulate spectral sensitivities on a range of timescales. These mechanisms include: (1) optical media that filter light, (2) variations in photoreceptor type and size to vary absorbance and sensitivity, and (3) changes in photoreceptor visual pigments to optimize peak sensitivity. The visual pigment changes can result from changes in chromophore or changes to the opsin. Opsin variation results from changes in opsin sequence, opsin expression or co-expression, and opsin gene duplications and losses. Here, we review visual diversity in a number of teleost groups where the structural and molecular mechanisms underlying their spectral sensitivities have been relatively well determined. Although we document considerable variability, this alone does not imply functional difference per se. We therefore highlight the need for more studies that examine species with known sensitivity differences, emphasizing behavioral experiments to test whether such differences actually matter in the execution of visual tasks that are relevant to the fish.
Vertebrate vision is accomplished through light-sensitive photopigments consisting of an opsin protein bound to a chromophore. In dim light, vertebrates generally rely on a single rod opsin rhodopsin ...1 (RH1) for obtaining visual information. By inspecting 101 fish genomes, we found that three deep-sea teleost lineages have independently expanded their
gene repertoires. Among these, the silver spinyfin (
) stands out as having the highest number of visual opsins in vertebrates (two cone opsins and 38 rod opsins). Spinyfins express up to 14
s (including the most blueshifted rod photopigments known), which cover the range of the residual daylight as well as the bioluminescence spectrum present in the deep sea. Our findings present molecular and functional evidence for the recurrent evolution of multiple rod opsin-based vision in vertebrates.
Phenotypic plasticity allows organisms to adapt quickly to local environmental conditions and could facilitate adaptive radiations. Cichlids have recently undergone an adaptive radiation in Lake ...Malawi where they inhabit diverse light environments and tune their visual sensitivity through differences in cone opsin expression. While cichlid opsin expression is known to be plastic over development, whether adults remain plastic is unknown. Adult plasticity in visual tuning could play a role in cichlid radiations by enabling survival in changing environments and facilitating invasion into novel environments. Here we examine the existence of and temporal changes in adult visual plasticity of two closely related species. In complementary experiments, wild adult Metriaclima mbenji from Lake Malawi were moved to the lab under UV‐deficient fluorescent lighting; while lab raised M. benetos were placed under UV‐rich lighting designed to mimic light conditions in the wild. Surprisingly, adult cichlids in both experiments showed significant changes in the expression of the UV‐sensitive single cone opsin, SWS1, in only 3 days. Modeling quantum catches in the light environments revealed a possible link between the light available to the SWS1 visual pigment and SWS1 expression. We conclude that adult cichlids can undergo rapid and significant changes in opsin expression in response to environmental light shifts that are relevant to their habitat and evolutionary history in Lake Malawi. This could have contributed to the rapid divergence characteristic of these fantastic fishes.
Vision mediates important behavioural tasks such as mate choice, escape from predators and foraging. In fish, photoreceptors are generally tuned to specific visual tasks and/or to their light ...environment, according to depth or water colour to ensure optimal performance. Evolutionary mechanisms acting on genes encoding opsin, the protein component of the photopigment, can influence the spectral sensitivity of photoreceptors. Opsin genes are known to respond to environmental conditions on a number of time scales, including short time frames due to seasonal variation, or through longer-term evolutionary tuning. There is also evidence for 'on-the-fly' adaptations in adult fish in response to rapidly changing environmental conditions; however, results are contradictory. Here, we investigated the ability of three reef fish species that belong to two ecologically distinct families, yellow-striped cardinalfish (
), Ambon damselfish (
) and lemon damselfish (
), to alter opsin gene expression as an adaptation to short-term (weeks to months) changes of environmental light conditions, and attempted to characterize the underlying expression regulation principles. We report the ability for all species to alter opsin gene expression within months and even a few weeks, suggesting that opsin expression in adult reef fish is not static. Furthermore, we found that changes in opsin expression in single cones generally occurred more rapidly than in double cones, and identified different responses of
opsin gene expression between the ecologically distinct reef fish families. Quantum catch correlation analysis suggested different regulation mechanisms for opsin expression dependent on gene class.
Color vision is the capacity to discriminate color regardless of brightness. It is essential for many fish species as they rely on color discrimination for numerous ecological tasks. The study of ...color vision is important because it can unveil the mechanisms that shape coloration patterns, visual system sensitivities and, hence, visual signals. In order to better understand the mechanisms underlying color vision, an integrative approach is necessary. This usually requires combining behavioral, physiological and genetic experiments with quantitative modeling, resulting in a distinctive characterization of the visual system. Here, we provide new data on the color vision of a rock-dwelling cichlid from Lake Malawi:
For this study we used a behavioral approach to demonstrate color vision through classical conditioning, complemented with modeling of color vision to estimate color contrast. For our experiments we took into account opsin coexpression and considered whether cichlids exhibit a dichromatic or a trichromatic visual system. Behavioral experiments confirmed color vision in
; most fish were significantly more likely to choose the trained over the distracter stimuli, irrespective of brightness. Our results are supported by visual modeling that suggests that cichlids are trichromats and achieve color vision through color opponency mechanisms, which are a result of three different photoreceptor channels. Our analyses also suggest that opsin coexpression can negatively affect perceived color contrast. This study is particularly relevant for research on the cichlid lineage because cichlid visual capabilities and coloration patterns are implicated in their adaptive radiation.
Animal visual systems adapt to environmental light on various timescales. In scotopic conditions, evolutionary time‐scale adaptations include spectral tuning to a narrower light spectrum, loss (or ...inactivation) of visual genes, and pure‐rod or rod‐dominated retinas. Some fishes inhabiting shallow coral reefs may show activity during the day and at night. It is unclear whether these fishes show adaptations typical of exclusively nocturnal or deep‐sea fishes, or of diurnally active shallow‐water species. Here, we investigated visual pigment diversity in cardinalfishes (Apogonidae). Most cardinalfishes are nocturnal foragers, yet they aggregate in multispecies groups in and around coral heads during the day, engaging in social and predator avoidance behaviours. We sequenced retinal transcriptomes of 28 species found on the Great Barrier Reef, assessed the diversity of expressed opsin genes and predicted the spectral sensitivities of resulting photopigments using sequence information. Predictions were combined with microspectrophotometry (MSP) measurements in seven cardinalfish species. Retinal opsin expression was rod opsin (RH1) dominated (>87%), suggesting the importance of scotopic vision. However, all species retained expression of multiple cone opsins also, presumably for colour vision. We found five distinct quantitative expression patterns among cardinalfishes, ranging from short‐wavelength‐shifted to long‐wavelength‐shifted. These results indicate that cardinalfishes are both well adapted to dim‐light conditions and have retained a sophisticated colour vision sense. Other reef fish families also show both nocturnal and diurnal activity while most are strictly one or the other. It will be interesting to compare these behavioural differences across different phylogenetic groups using the criteria and methods developed here.
The opsin genes of amazonian cichlids Escobar‐Camacho, Daniel; Ramos, Erica; Martins, Cesar ...
Molecular ecology,
March 2017, Volume:
26, Issue:
5
Journal Article
Peer reviewed
Open access
Vision is a critical sense for organismal survival with visual sensitivities strongly shaped by the environment. Some freshwater fishes with a Gondwanan origin are distributed in both South American ...rivers including the Amazon and African rivers and lakes. These different habitats likely required adaptations to murky and clear environments. In this study, we compare the molecular basis of Amazonian and African cichlid fishes’ visual systems. We used next‐generation sequencing of genomes and retinal transcriptomes to examine three Amazonian cichlid species. Genome assemblies revealed six cone opsin classes (SWS1, SWS2B, SWS2A, RH2B, RH2A and LWS) and rod opsin (RH1). However, the functionality of these genes varies across species with different pseudogenes found in different species. Our results support evidence of an RH2A gene duplication event that is shared across both cichlid groups, but which was probably followed by gene conversion. Transcriptome analyses show that Amazonian species mainly express three opsin classes (SWS2A, RH2A and LWS), which likely are a good match to the long‐wavelength‐oriented light environment of the Amazon basin. Furthermore, analysis of amino acid sequences suggests that the short‐wavelength‐sensitive genes (SWS2B, SWS2A) may be under selective pressures to shift their spectral properties to a longer‐wavelength visual palette. Our results agree with the ‘sensitivity hypothesis’ where the light environment causes visual adaptation. Amazonian cichlid visual systems are likely adapting through gene expression, gene loss and possibly spectral tuning of opsin sequences. Such mechanisms may be shared across the Amazonian fish fauna.
see also the Perspective by Owens and Rennison
•Cichlid visual sensitivities vary by changing cornea and lens transmission, photoreceptor densities, and photoreceptor sensitivities•Cichlid photoreceptor sensitivities shift through changes to ...chromophore, opsin gene sequence, opsin gene expression and opsin gene loss•Sensitivity differences are linked to differences in ecology including foraging and light environment•Cichlids are a powerful example of how the comparative approach can unravel the proximate and ultimate causes of visual system variation
The family Cichlidae contains approximately 2000 species that live in diverse freshwater habitats including murky lakes, turbid rivers, and clear lakes from both the Old and New Worlds. Their visual systems are similarly diverse and have evolved specific sensitivities that differ along several axes of variation. Variation in cornea and lens transmission affect which wavelengths reach the retina. Variation in photoreceptor number and distribution affect brightness sensitivity, spectral sensitivity and resolution. Probably their most dynamic characteristic is the variation in visual pigment peak sensitivities. Visual pigments can be altered through changes in chromophore, opsin sequence and opsin expression. Opsin expression varies by altering which of the seven available cone opsins in their genomes are turned on. These opsins can even be coexpressed to produce seemingly infinitely tunable cone sensitivities. Both chromophore and opsin expression can vary on either rapid (hours or days), slower (seasonal or ontogenetic) or evolutionary timescales. Such visual system shifts have enabled cichlids to adapt to different habitats and foraging styles. Through both short term plasticity and longer evolutionary adaptations, cichlids have proven to be ecologically successful and an excellent model for studying organismal adaptation.
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