Developmental dynamics of cone photoreceptors in the eel

Background: Many fish alter their expressed visual pigments during development. The number of retinal opsins expressed and their type is normally related to the environment in which they live. Eels are known to change the expression of their rod opsins as they mature, but might they also change the expression of their cone opsins?Results: The Rh2 and Sws2 opsin sequences from the European Eel were isolated, sequenced and expressed in vitro for an accurate measurement of their lambda(max) values. In situ hybridisation revealed that glass eels express only rh2 opsin in their cone photoreceptors, while larger yellow eels continue to express rh2 opsin in the majority of their cones, but also have <5% of cones which express sws2 opsin. Silver eels showed the same expression pattern as the larger yellow eels. This observation was confirmed by qPCR (quantitative polymerase chain reaction).Conclusions: Larger yellow and silver European eels express two different cone opsins, rh2 and sws2. This work demonstrates that only the Rh2 cone opsin is present in younger fish (smaller yellow and glass), the sws2 opsin being expressed additionally only by older fish and only in <5% of cone cells

Rapid adaptive evolution of colour vision in the threespine stickleback radiation.

Vision is a sensory modality of fundamental importance for many animals, aiding in foraging, detection of predators and mate choice. Adaptation to local ambient light conditions is thought to be commonplace, and a match between spectral sensitivity and light spectrum is predicted. We use opsin gene expression to test for local adaptation and matching of spectral sensitivity in multiple independent lake populations of threespine stickleback populations derived since the last ice age from an ancestral marine form. We show that sensitivity across the visual spectrum is shifted repeatedly towards longer wavelengths in freshwater compared with the ancestral marine form. Laboratory rearing suggests that this shift is largely genetically based. Using a new metric, we found that the magnitude of shift in spectral sensitivity in each population corresponds strongly to the transition in the availability of different wavelengths of light between the marine and lake environments. We also found evidence of local adaptation by sympatric benthic and limnetic ecotypes to different light environments within lakes. Our findings indicate rapid parallel evolution of the visual system to altered light conditions. The changes have not, however, yielded a close matching of spectrum-wide sensitivity to wavelength availability, for reasons we discuss

An EvoDevo Study of Salmonid Visual Opsin Dynamics and Photopigment Spectral Sensitivity

Salmonids are ideal models as many species follow a distinct developmental program from demersal eggs and a large yolk sac to hatching at an advanced developmental stage. Further, these economically important teleosts inhabit both marine- and freshwaters and experience diverse light environments during their life histories. At a genome level, salmonids have undergone a salmonid-specific fourth whole genome duplication event (Ss4R) compared to other teleosts that are already more genetically diverse compared to many non-teleost vertebrates. Thus, salmonids display phenotypically plastic visual systems that appear to be closely related to their anadromous migration patterns. This is most likely due to a complex interplay between their larger, more gene-rich genomes and broad spectrally enriched habitats; however, the molecular basis and functional consequences for such diversity is not fully understood. This study used advances in genome sequencing to identify the repertoire and genome organization of visual opsin genes (those primarily expressed in retinal photoreceptors) from six different salmonids [Atlantic salmon (Salmo salar), brown trout (Salmo trutta), Chinook salmon (Oncorhynchus tshawytcha), coho salmon (Oncorhynchus kisutch), rainbow trout (Oncorhynchus mykiss), and sockeye salmon (Oncorhynchus nerka)] compared to the northern pike (Esox lucius), a closely related non-salmonid species. Results identified multiple orthologues for all five visual opsin classes, except for presence of a single short-wavelength-sensitive-2 opsin gene. Several visual opsin genes were not retained after the Ss4R duplication event, which is consistent with the concept of salmonid rediploidization. Developmentally, transcriptomic analyzes of Atlantic salmon revealed differential expression within each opsin class, with two of the long-wavelength-sensitive opsins not being expressed before first feeding. Also, early opsin expression in the retina was located centrally, expanding dorsally and ventrally as eye development progressed, with rod opsin being the dominant visual opsin post-hatching. Modeling by spectral tuning analysis and atomistic molecular simulation, predicted the greatest variation in the spectral peak of absorbance to be within the Rh2 class, with a ∼40 nm difference in λmax values between the four medium-wavelength-sensitive photopigments. Overall, it appears that opsin duplication and expression, and their respective spectral tuning profiles, evolved to maximize specialist color vision throughout an anadromous lifecycle, with some visual opsin genes being lost to tailor marine-based vision.publishedVersio

Mechanistic insights into the evolution of the differential expression of tandemly arrayed cone opsin genes in zebrafish

The genome of many organisms contains several loci consisting of duplicated genes that are arrayed in tandem. The daughter genes produced by duplication typically exhibit differential expression patterns with each other or otherwise experience pseudogenization. Remarkably, opsin genes in fish are preserved after many duplications in different lineages. This fact indicates that fish opsin genes are characterized by a regulatory mechanism that could intrinsically facilitate the differentiation of the expression patterns. However, little is known about the mechanisms that underlie the differential expression patterns or how they were established during evolution. The loci of green (RH2)- and red (LWS)-sensitive cone opsin genes in zebrafish have been used as model systems to study the differential regulation of tandemly arrayed opsin genes. Over a decade of studies have uncovered several mechanistic features that might have assisted the differentiation and preservation of duplicated genes. Furthermore, recent progress in the understanding of the transcriptional process in general has added essential insights. In this article, the current understanding of the transcriptional regulation of differentially expressed tandemly arrayed cone opsin genes in zebrafish is summarized and a possible evolutionary scenario that could achieve this differentiation is discussed

Cichlids as a model for the evolution of visual sensitivity

The cichlid fishes of East Africa are the most ecologically diverse radiation of recent vertebrates. These highly visual fish live in habitats ranging from turbid rivers to clear lakes. They have evolved to exploit an astounding array of foraging strategies. The combination of phenotypic diversity and varied environmental conditions makes the cichlid system ideal for the examination of the relationship between ecology and the evolution of visual sensitivity. In this dissertation, I explore several aspects of this relationship. In Chapter 1, I compare the opsin gene sequences from 17 African cichlid species that have evolved in either clear or turbid light environments. I identify statistical evidence of molecular adaptation. I also find evidence of differences in the relative rates of substitution across clear and turbid lineages. When patterns of amino acid substitution are compared to possible tuning sites, only the ultraviolet sensitive SWS1 class have patterns of substitution that are consistent with photic environment-driven evolution. In Chapter 2, I determine the peak absorbances of in vitro expressed pigments for all seven Nile tilapia cone opsin genes and chart opsin expression across ontogeny. Each gene is found to encode a distinct photopigment. Despite the expression of a limited subset of opsin genes in adults, each opsin was found to be expressed at some point during ontogeny. In Chapter 3, I use MSP and real-time RT-PCR to characterize the differences in visual sensitivity among one of Lake Malawi\u27s most species rich genera, Labidochromis. This study suggests that visual sensitivity is quite labile and can change during the evolution of closely related species. In chapter 4, I examine the distribution of retained opsin gene duplicates among all fish opsins sequenced to date. Duplicates are found differentially across opsin classes. Overall, the majority of retained gene duplicates began to accumulate around the time of the radiation of higher teleosts. Finally in Chapter 5, I highlight ways in which the cichlid system might be especially useful in relating ecology and vision. This includes identifying how visual sensitivity has been shaped by specific foraging strategies and how this affects the long-term evolution of the cone opsin family

A Fish Eye Out of Water: Ten Visual Opsins in the Four-Eyed Fish, Anableps anableps

The “four-eyed” fish Anableps anableps has numerous morphological adaptations that enable above and below-water vision. Here, as the first step in our efforts to identify molecular adaptations for aerial and aquatic vision in this species, we describe the A. anableps visual opsin repertoire. We used PCR, cloning, and sequencing to survey cDNA using unique primers designed to amplify eight sequences from five visual opsin gene subfamilies, SWS1, SWS2, RH1, RH2, and LWS. We also used Southern blotting to count opsin loci in genomic DNA digested with EcoR1 and BamH1. Phylogenetic analyses confirmed the identity of all opsin sequences and allowed us to map gene duplication and divergence events onto a tree of teleost fish. Each of the gene-specific primer sets produced an amplicon from cDNA, indicating that A. anableps possessed and expressed at least eight opsin genes. A second PCR-based survey of genomic and cDNA uncovered two additional LWS genes. Thus, A. anableps has at least ten visual opsins and all but one were expressed in the eyes of the single adult surveyed. Among these ten visual opsins, two have key site haplotypes not found in other fish. Of particular interest is the A. anableps-specific opsin in the LWS subfamily, S180γ, with a SHYAA five key site haplotype. Although A. anableps has a visual opsin gene repertoire similar to that found in other fishes in the suborder Cyprinodontoidei, the LWS opsin subfamily has two loci not found in close relatives, including one with a key site haplotype not found in any other fish species. A. anableps opsin sequence data will be used to design in situ probes allowing us to test the hypothesis that opsin gene expression differs in the distinct ventral and dorsal retinas found in this species

Opsin expression predicts male nuptial color in threespine stickleback.

Theoretical models of sexual selection suggest that male courtship signals can evolve through the build-up of genetic correlations between the male signal and female preference. When preference is mediated via increased sensitivity of the signal characteristics, correlations between male signal and perception/sensitivity are expected. When signal expression is limited to males, we would expect to find signal-sensitivity correlations in males. Here, we document such a correlation within a breeding population of threespine stickleback mediated by differences in opsin expression. Males with redder nuptial coloration express more long-wavelength-sensitive (LWS) opsin, making them more sensitive to orange and red. This correlation is not an artifact of shared tuning to the optical microhabitat. Such correlations are an essential feature of many models of sexual selection, and our results highlight the potential importance of opsin expression variation as a substrate for signal-preference evolution. Finally, these results suggest a potential sensory mechanism that could drive negative frequency-dependent selection via male-male competition and thus maintain variation in male nuptial color