Long-wavelength-sensitive (lws) opsin gene expression, foraging and visual communication in coral reef fishes.

Coral reef fishes are diverse in ecology and behaviour and show remarkable colour variability. Investigating the visual pigment gene (opsin) expression in these fishes makes it possible to associate their visual genotype and phenotype (spectral sensitivities) to visual tasks, such as feeding strategy or conspecific detection. By studying all major damselfish clades (Pomacentridae) and representatives from five other coral reef fish families, we show that the long-wavelength-sensitive (lws) opsin is highly expressed in algivorous and less or not expressed in zooplanktivorous species. Lws is also upregulated in species with orange/red colours (reflectance >520 nm) and expression is highest in orange/red-coloured algivores. Visual models from the perspective of a typical damselfish indicate that sensitivity to longer wavelengths does enhance the ability to detect the red to far-red component of algae and orange/red-coloured conspecifics, possibly enabling social signalling. Character state reconstructions indicate that in the early evolutionary history of damselfishes, there was no lws expression and no orange/red coloration. Omnivory was most often the dominant state. Although herbivory was sometimes dominant, zooplanktivory was never dominant. Sensitivity to long wavelength (increased lws expression) only emerged in association with algivory but never with zooplanktivory. Higher lws expression is also exploited by social signalling in orange/red, which emerged after the transition to algivory. Although the relative timing of traits may deviate by different reconstructions and alternative explanations are possible, our results are consistent with sensory bias whereby social signals evolve as a correlated response to natural selection on sensory system properties in other contexts.

A novel exome probe set captures phototransduction genes across birds (Aves) enabling efficient analysis of vision evolution.

The diversity of avian visual phenotypes provides a framework for studying mechanisms of trait diversification generally, and the evolution of vertebrate vision, specifically. Previous research has focused on opsins, but to fully understand visual adaptation, we must study the complete phototransduction cascade (PTC). Here, we developed a probe set that captures exonic regions of 46 genes representing the PTC and other light responses. For a subset of species, we directly compared gene capture between our probe set and low-coverage whole genome sequencing (WGS), and we discuss considerations for choosing between these methods. Finally, we developed a unique strategy to avoid chimeric assembly by using "decoy" reference sequences. We successfully captured an average of 64% of our targeted exome in 46 species across 14 orders using the probe set and had similar recovery using the WGS data. Compared to WGS or transcriptomes, our probe set: (1) reduces sequencing requirements by efficiently capturing vision genes, (2) employs a simpler bioinformatic pipeline by limiting required assembly and negating annotation, and (3) eliminates the need for fresh tissues, enabling researchers to leverage existing museum collections. We then utilized our vision exome data to identify positively selected genes in two evolutionary scenarios-evolution of night vision in nocturnal birds and evolution of high-speed vision specific to manakins (Pipridae). We found parallel positive selection of SLC24A1 in both scenarios, implicating the alteration of rod response kinetics, which could improve color discrimination in dim light conditions and/or facilitate higher temporal resolution.

Chromosome-level assembly of southern catfish (silurus meridionalis) provides insights into visual adaptation to nocturnal and benthic lifestyles.

The Southern catfish (Silurus meridionalis) is a nocturnal and benthic freshwater fish endemic to the Yangtze River and its tributaries. In this study, we constructed a chromosome-level draft genome of S. meridionalis using 69.7-Gb Nanopore long reads and 49.5-Gb Illumina short reads. The genome assembly was 741.2 Mb in size with a contig N50 of 13.19 Mb. An additional 116.4 Gb of Bionano and 77.4 Gb of Hi-C data were applied to assemble contigs into scaffolds and further into 29 chromosomes, resulting in a 738.9-Mb genome with a scaffold N50 of 28.04 Mb. A total of 22,965 protein-coding genes were predicted from the genome with 22,519 (98.06%) genes functionally annotated. Comparative genomic and transcriptomic analyses revealed a rod-dominated visual system which was responsible for scotopic vision. The absence of cone opsins SWS1 and SWS2 resulted in the lack of ultraviolet and blue violet sensitivity. Mutations at key amino acid sites of RH1.1, RH1.2 and RH2 resulted in spectral tuning good for dim light vision and narrow colour vision. A higher expression level of rod phototransduction genes than that of cone genes and higher rod-to-cone ratio led to higher optical sensitivity under dim light conditions. In addition, analysis of the genes involved in eye morphogenesis and development revealed the loss of some conserved noncoding elements, which might be associated with the small eyes in catfish. Together, our study provides important clues for the adaptation of the catfish visual system to the nocturnal and benthic lifestyles. The draft genome of S. meridionalis represents a valuable resource for studies of the molecular mechanisms of ecological adaptation.

Movement of transposable elements contributes to cichlid diversity.

African cichlid fishes are a prime model for studying speciation mechanisms. Despite the development of extensive genomic resources, it has been difficult to determine which sources of genetic variation are responsible for cichlid phenotypic variation. One of their most variable phenotypes is visual sensitivity, with some of the largest spectral shifts among vertebrates. These shifts arise primarily from differential expression of seven cone opsin genes. By mapping expression quantitative trait loci (eQTL) in intergeneric crosses of Lake Malawi cichlids, we previously identified four causative genetic variants that correspond to indels in the promoters of either key transcription factors or an opsin gene. In this comprehensive study, we show that these indels are the result of the movement of transposable elements (TEs) that correlate with opsin expression variation across the Malawi flock. In tracking the evolutionary history of these particular indels, we found they are endemic to Lake Malawi, suggesting that these TEs are recently active and are segregating within the Malawi cichlid lineage. However, an independent indel has arisen at a similar genomic location in one locus outside of the Malawi flock. The convergence in TE movement suggests these loci are primed for TE insertion and subsequent deletions. Increased TE mobility may be associated with interspecific hybridization, which disrupts mechanisms of TE suppression. This might provide a link between cichlid hybridization and accelerated regulatory variation. Overall, our study suggests that TEs may be an important driver of key regulatory changes, facilitating rapid phenotypic change and possibly speciation in African cichlids.

Visual pigment evolution in Characiformes: The dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning.

Vision represents an excellent model for studying adaptation, given the genotype-to-phenotype map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light, making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we showcase the visual system evolution of neotropical Characiformes and the spectral tuning mechanisms they exhibit to modulate their visual sensitivities. Such mechanisms include gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1 /A2 -chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiform's entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS- and RH1-duplicates originated from a teleost specific whole-genome duplication as well as characiform-specific duplication events. Both LWS-opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS-paralogues has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. Furthermore, characiforms' colour vision is based on the expression of both LWS-paralogues and SWS2. Finally, we found interspecific and intraspecific variation in A1 /A2 -chromophores proportions, correlating with the light environment. These multiple mechanisms may be a result of the diverse visual environments where Characiformes have evolved.

Axes of visual adaptation in the ecologically diverse family Cichlidae.

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.

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes.

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.

Tbx2a Modulates Switching of RH2 and LWS Opsin Gene Expression.

Sensory systems are tuned by selection to maximize organismal fitness in particular environments. This tuning has implications for intraspecies communication, the maintenance of species boundaries, and speciation. Tuning of color vision largely depends on the sequence of the expressed opsin proteins. To improve tuning of visual sensitivities to shifts in habitat or foraging ecology over the course of development, many organisms change which opsins are expressed. Changes in this developmental sequence (heterochronic shifts) can create differences in visual sensitivity among closely related species. The genetic mechanisms by which these developmental shifts occur are poorly understood. Here, we use quantitative trait locus analyses, genome sequencing, and gene expression studies in African cichlid fishes to identify a role for the transcription factor Tbx2a in driving a switch between long wavelength sensitive (LWS) and Rhodopsin-like (RH2) opsin expression. We identify binding sites for Tbx2a in the LWS promoter and the highly conserved locus control region of RH2 which concurrently promote LWS expression while repressing RH2 expression. We also present evidence that a single change in Tbx2a regulatory sequence has led to a species difference in visual tuning, providing the first mechanistic model for the evolution of rapid switches in sensory tuning. This difference in visual tuning likely has important roles in evolution as it corresponds to differences in diet, microhabitat choice, and male nuptial coloration.

Visual adaptation could aid sympatric speciation in a deep crater lake.

Allopatric speciation was originally suggested to be the primary mechanism of animal speciation (Mayr, 1942; Figure 1). During allopatric speciation, populations diverge when gene flow is reduced across significant biogeographic barriers. Sympatric speciation, where species diverge while inhabiting the same location, was thought to be essentially impossible. However, the advent of theoretical models followed by new experimental evidence made sympatric speciation more plausible (Via, 2001). The cichlid fishes of Barombi Mbo, a small crater lake in western Cameroon, became one of the most widely accepted examples of sympatric speciation (Schliewen, Tautz, & Paabo, 1994). Although the phylogenetic history of this clade is not quite as simple as originally thought, it remains one of the best examples of sympatric speciation (Richards, Poelstra, & Martin, 2018). However, little is known about the molecular mechanisms contributing to the splitting of these species in situ. In a From the Cover article in this issue of Molecular Ecology, Musilova et al. (2019) focus on the diversity of visual systems among these fishes. They identify genetic changes associated with several aspects of visual adaptation that may have contributed to the ecological specialization and sympatric speciation of cichlids in this lake.

A detailed investigation of the visual system and visual ecology of the Barrier Reef anemonefish, Amphiprion akindynos.

Vision plays a major role in the life of most teleosts, and is assumingly well adapted to each species ecology and behaviour. Using a multidisciplinary approach, we scrutinised several aspects of the visual system and ecology of the Great Barrier Reef anemonefish, Amphiprion akindynos, including its orange with white patterning, retinal anatomy and molecular biology, its symbiosis with anemones and sequential hermaphroditism. Amphiprion akindynos possesses spectrally distinct visual pigments and opsins: one rod opsin, RH1 (498 nm), and five cone opsins, SWS1 (370 nm), SWS2B (408 nm), RH2B (498 nm), RH2A (520 nm), and LWS (554 nm). Cones were arranged in a regular mosaic with each single cone surrounded by four double cones. Double cones mainly expressed RH2B (53%) in one member and RH2A (46%) in the other, matching the prevailing light. Single cones expressed SWS1 (89%), which may serve to detect zooplankton, conspecifics and the host anemone. Moreover, a segregated small fraction of single cones coexpressed SWS1 with SWS2B (11%). This novel visual specialisation falls within the region of highest acuity and is suggested to increase the chromatic contrast of Amphiprion akindynos colour patterns, which might improve detection of conspecifics.

Color discrimination thresholds in a cichlid fish: Metriaclima benetos.

Color vision is essential for animals as it allows them to detect, recognize and discriminate between colored objects. Studies analyzing color vision require an integrative approach, combining behavioral experiments, physiological models and quantitative analyses of photoreceptor stimulation. Here, we demonstrate, for the first time, the limits of chromatic discrimination in Metriaclima benetos, a rock-dwelling cichlid from Lake Malawi, using behavioral experiments and visual modeling. Fish were trained to discriminate between colored stimuli. Color discrimination thresholds were quantified by testing fish chromatic discrimination between the rewarded stimulus and distracter stimuli that varied in chromatic distance (ΔS). This was done under fluorescent lights alone and with additional violet lights. Our results provide two main outcomes. First, cichlid color discrimination thresholds correspond with predictions from the receptor noise limited (RNL) model but only if we assume a Weber fraction higher than the typical value of 5%. Second, cichlids may exhibit limited color constancy under certain lighting conditions as most individuals failed to discriminate colors when violet light was added. We further used the color discrimination thresholds obtained from these experiments to model color discrimination of actual fish colors and backgrounds under natural lighting for Lake Malawi. We found that, for M. benetos, blue is most chromatically contrasting against yellows and space-light, which might be important for discriminating male nuptial colorations and detecting males against the background. This study highlights the importance of lab-based behavioral experiments in understanding color vision and in parameterizing the assumptions of the RNL vision model for different species.

Diurnal variation in opsin expression and common housekeeping genes necessitates comprehensive normalization methods for quantitative real-time PCR analyses.

To determine the visual sensitivities of an organism of interest, quantitative reverse transcription-polymerase chain reaction (qRT-PCR) is often used to quantify expression of the light-sensitive opsins in the retina. While qRT-PCR is an affordable, high-throughput method for measuring expression, it comes with inherent normalization issues that affect the interpretation of results, especially as opsin expression can vary greatly based on developmental stage, light environment or diurnal cycles. We tested for diurnal cycles of opsin expression over a period of 24 hr at 1-hr increments and examined how normalization affects a data set with fluctuating expression levels using qRT-PCR and transcriptome data from the retinae of the cichlid Pelmatolapia mariae. We compared five methods of normalizing opsin expression relative to (a) the average of three stably expressed housekeeping genes (Ube2z, EF1-α and ß-actin), (b) total RNA concentration, (c) GNAT2, (the cone-specific subunit of transducin), (d) total opsin expression and (e) only opsins expressed in the same cone type. Normalizing by proportion of cone type produced the least variation and would be best for removing time-of-day variation. In contrast, normalizing by housekeeping genes produced the highest daily variation in expression and demonstrated that the peak of cone opsin expression was in the late afternoon. A weighted correlation network analysis showed that the expression of different cone opsins follows a very similar daily cycle. With the knowledge of how these normalization methods affect opsin expression data, we make recommendations for designing sampling approaches and quantification methods based upon the scientific question being examined.

Vision using multiple distinct rod opsins in deep-sea fishes.

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 RH1 gene repertoires. Among these, the silver spinyfin (Diretmus argenteus) stands out as having the highest number of visual opsins in vertebrates (two cone opsins and 38 rod opsins). Spinyfins express up to 14 RH1s (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.

Cardinalfishes (Apogonidae) show visual system adaptations typical of nocturnally and diurnally active fish.

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.

Chromosome-scale assemblies reveal the structural evolution of African cichlid genomes.

BACKGROUND: African cichlid fishes are well known for their rapid radiations and are a model system for studying evolutionary processes. Here we compare multiple, high-quality, chromosome-scale genome assemblies to elucidate the genetic mechanisms underlying cichlid diversification and study how genome structure evolves in rapidly radiating lineages. RESULTS: We re-anchored our recent assembly of the Nile tilapia (Oreochromis niloticus) genome using a new high-density genetic map. We also developed a new de novo genome assembly of the Lake Malawi cichlid, Metriaclima zebra, using high-coverage Pacific Biosciences sequencing, and anchored contigs to linkage groups (LGs) using 4 different genetic maps. These new anchored assemblies allow the first chromosome-scale comparisons of African cichlid genomes. Large intra-chromosomal structural differences (∼2-28 megabase pairs) among species are common, while inter-chromosomal differences are rare (<10 megabase pairs total). Placement of the centromeres within the chromosome-scale assemblies identifies large structural differences that explain many of the karyotype differences among species. Structural differences are also associated with unique patterns of recombination on sex chromosomes. Structural differences on LG9, LG11, and LG20 are associated with reduced recombination, indicative of inversions between the rock- and sand-dwelling clades of Lake Malawi cichlids. M. zebra has a larger number of recent transposable element insertions compared with O. niloticus, suggesting that several transposable element families have a higher rate of insertion in the haplochromine cichlid lineage. CONCLUSION: This study identifies novel structural variation among East African cichlid genomes and provides a new set of genomic resources to support research on the mechanisms driving cichlid adaptation and speciation.

Variable vision in variable environments: the visual system of an invasive cichlid (Cichla monoculus) in Lake Gatun, Panama.

An adaptive visual system is essential for organisms inhabiting new or changing light environments. The Panama Canal exhibits such variable environments owing to its anthropogenic origin and current human activities. Within the Panama Canal, Lake Gatun harbors several exotic fish species including the invasive peacock bass (Cichla monoculus), a predatory Amazonian cichlid. In this research, through spectral measurements and molecular and physiological experiments, we studied the visual system of C. monoculus and its adaptive capabilities. Our results suggest that (1) Lake Gatun is a highly variable environment, where light transmission changes throughout the canal waterway, and that (2) C. monoculus has several visual adaptations suited for this red-shifted light environment. Cichla monoculus filters short wavelengths (∼400 nm) from the environment through its ocular media and tunes its visual sensitivities to the available light through opsin gene expression. More importantly, based on shifts in spectral sensitivities of photoreceptors alone, and on transcriptome analysis, C. monoculus exhibits extreme intraspecific variation in the use of vitamin A1/A2 chromophore in their photoreceptors. Fish living in turbid water had higher proportions of vitamin A2, shifting sensitivities to longer wavelengths, than fish living in clear water. Furthermore, we also found variation in retinal transcriptomes, where fish from turbid and clear waters exhibited differentially expressed genes that vary greatly in their function. We suggest that this phenotypic plasticity has been key in the invasion success of C. monoculus.

Multiple trans QTL and one cis-regulatory deletion are associated with the differential expression of cone opsins in African cichlids.

BACKGROUND: Dissecting the genetic basis of phenotypic diversity is one of the fundamental goals in evolutionary biology. Despite growing evidence for gene expression divergence being responsible for the evolution of complex traits, knowledge about the proximate genetic causes underlying these traits is still limited. African cichlids have diverse visual systems, with different species expressing different combinations of seven cone opsin genes. Using opsin expression variation in African cichlids as a model for gene expression evolution, this study aims to investigate the genetic architecture of opsin expression divergence in this group. RESULTS: Results from a genome-wide linkage mapping on the F2 progeny of an intergeneric cross, between two species with differential opsin expression show that opsins in Lake Malawi cichlids are controlled by multiple quantitative trait loci (QTLs). Most of these QTLs are located in trans to the opsins except for one cis-QTL for SWS1 on LG17. A closer look at this major QTL revealed the presence of a 691 bp deletion in the promoter of the SWS1 opsin (located 751 bp upstream of the start site) that is associated with a decrease in its expression. Phylogenetic footprinting indicates that the region spanning the deletion harbors a microRNA miR-729 and a conserved non-coding element (CNE) that also occurs in zebrafish and other teleosts. This suggests that the deletion might contain ancestrally preserved regulators that have been tuned for SWS1 gene expression in Lake Malawi. While this deletion is not common, it does occur in several other species within the lake. CONCLUSIONS: Differential expression of cichlid opsins is associated with multiple overlapping QTL, with all but one in trans to the opsins they regulate. The one cis-acting factor is a deletion in the promoter of the SWS1 opsin, suggesting that ancestral polymorphic deletions may contribute to cichlid's visual diversity. In addition to expanding our understanding of the molecular landscape of opsin expression in African cichlids, this study sheds light on the molecular mechanisms underlying phenotypic variation in natural populations.

Short-term colour vision plasticity on the reef: changes in opsin expression under varying light conditions differ between ecologically distinct fish species.

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 (Ostorhinchus cyanosoma), Ambon damselfish (Pomacentrus amboinensis) and lemon damselfish (Pomacentrus moluccensis), 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 RH2 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.

Opsin Expression in the Central Nervous System of the Mantis Shrimp Neogonodactylus oerstedii.

Visual pigments, each composed of an opsin protein covalently bound to a chromophore molecule, confer light sensitivity for vision. The eyes of some species of stomatopod crustaceans, or mantis shrimp, can express dozens of different opsin genes. The opsin diversity, along with spectral filters and unique tripartite eye structure, bestow upon stomatopods unusually complex visual systems. Although opsins are found in tissues outside typical image-forming eyes in other animals, extraocular opsin expression in stomatopods, animals well known for their diversity of opsins, was unknown. Caudal photoreception in the central nervous system of decapod crustaceans, a group closely related to stomatopod crustaceans, is thought to be opsin based. However, electrophysiological data suggest that stomatopods do not have caudal photoreceptors. In this study, we identified mRNAs that could encode four different opsins and several components of a potential Gq-mediated phototransduction pathway in the central nervous system of the Caribbean mantis shrimp Neogonodactylus oerstedii. The four opsins are abundantly expressed in the cerebral ganglion, or brain, with little or no expression in the remainder of the ventral nerve cord. Our data suggest that there are previously undiscovered cerebral photoreceptors in stomatopods.

Adult plasticity in African cichlids: Rapid changes in opsin expression in response to environmental light differences.

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.