skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Light environment and seasonal variation in the visual system of the red shiner ( Cyprinella lutrensis )
Abstract The light environment underwater can vary dramatically over space and time, challenging the visual systems of aquatic organisms. To meet these challenges, many species shift their spectral sensitivities through changes in visual pigment chromophore and opsin expression. The red shiner (Cyprinella lutrensis) is a cyprinid minnow species that has rapidly expanded its range throughout North America and inhabits a wide range of aquatic habitats. We hypothesized that visual system plasticity has contributed to the red shiner’s success. We investigated plasticity in chromophore usage and opsin expression by collecting red shiners from three Oklahoma creeks that vary in turbidity throughout the year. We characterized the light environment by spectroradiometry, measured chromophore composition of the eyes with high performance liquid chromatography, characterized CYP27C1 enzyme function through heterologous expression, and examined ocular gene expression by RNA sequencing andde novotranscriptome assembly. We observed significantly higher proportions of the long- wavelength shifted A2chromophore in the eyes of fish from the turbid site and in samples collected in winter, suggesting that there may be a temperature-dependent trade-off between chromophore-based spectral tuning and chromophore-related noise. Opsin expression varied between turbid and clear creeks, but did not align with light environment as expected, and the magnitude of these differences was limited compared to the differences in chromophore composition. We confirmed that red shinerCYP27C1catalyzes the conversion of A1to A2, but the ocular expression ofCYP27C1was not well correlated with A2levels in the eye, suggesting conversion may be occurring outside of the eye.  more » « less
Award ID(s):
2037739
PAR ID:
10520201
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
bioRxiv
Date Published:
Format(s):
Medium: X
Institution:
bioRxiv
Sponsoring Org:
National Science Foundation
More Like this
  1. The light environment underwater can vary dramatically over space and time, challenging the visual systems of aquatic organisms. To meet these challenges, many species shift their spectral sensitivities through changes in visual pigment chromophore composition and opsin expression. The red shiner (Cyprinella lutrensis) is a North American cyprinid minnow species that inhabits waters ranging widely in turbidity and temperature. We hypothesized that the visual system of the red shiner is plastic with chromophore composition and opsin expression varying in response to the environment. To test this hypothesis, we collected red shiners throughout the year from three Oklahoma creeks that vary in turbidity. We characterized the light environment by spectroradiometry, measured chromophore composition of the eyes with high performance liquid chromatography, characterized the mechanisms of chromophore metabolism, and examined ocular gene expression by RNA sequencing and de novo transcriptome assembly. We observed significantly higher proportions of the long-wavelength shifted A2 chromophore in the eyes of fish from the turbid site and in samples collected in winter, suggesting that there may be a temperature-dependent trade-off between chromophore-based spectral tuning and chromophore-related noise. Opsin expression varied between turbid and clear creeks, but did not align with light environment as expected, and the magnitude of these differences was limited compared to the differences in chromophore composition. We confirmed that red shiner CYP27C1 catalyzes the conversion of A1 to A2, but the ocular expression of CYP27C1 was not well correlated with A2 levels in the eye, suggesting conversion may be occurring outside of the eye. 
    more » « less
  2. Abstract BackgroundDifferences in morphology, ecology, and behavior through ontogeny can result in opposing selective pressures at different life stages. Most animals, however, transition through two or more distinct phenotypic phases, which is hypothesized to allow each life stage to adapt more freely to its ecological niche. How this applies to sensory systems, and in particular how sensory systems adapt across life stages at the molecular level, is not well understood. Here, we used whole-eye transcriptomes to investigate differences in gene expression between tadpole and juvenile southern leopard frogs (Lithobates sphenocephalus), which rely on vision in aquatic and terrestrial light environments, respectively. Because visual physiology changes with light levels, we also tested the effect of light and dark exposure. ResultsWe found 42% of genes were differentially expressed in the eyes of tadpoles versus juveniles and 5% for light/dark exposure. Analyses targeting a curated subset of visual genes revealed significant differential expression of genes that control aspects of visual function and development, including spectral sensitivity and lens composition. Finally, microspectrophotometry of photoreceptors confirmed shifts in spectral sensitivity predicted by the expression results, consistent with adaptation to distinct light environments. ConclusionsOverall, we identified extensive expression-level differences in the eyes of tadpoles and juveniles related to observed morphological and physiological changes through metamorphosis and corresponding adaptive shifts to improve vision in the distinct aquatic and terrestrial light environments these frogs inhabit during their life cycle. More broadly, these results suggest that decoupling of gene expression can mediate the opposing selection pressures experienced by organisms with complex life cycles that inhabit different environmental conditions throughout ontogeny. 
    more » « less
  3. Cubomedusae, or box jellyfish, have a complex visual system comprising 24 eyes of four types. Like other cnidarians, their photoreceptor cells are ciliary in morphology, and a range of different techniques together show that at least two of the eye types—the image-forming upper and lower lens eyes—express opsin as the photopigment. The photoreceptors of these two eye types express the same opsin ( Tc LEO ), which belongs to the cnidarian-specific clade cnidops. Interestingly, molecular work has found a high number of opsin genes in box jellyfish, especially in the Caribbean species Tripedalia cystophora , most of which are of unknown function. In the current study, we raised antibodies against three out of five opsins identified from transcriptomic data from T. cystophora and used them to map the expression patterns. These expression patterns suggest one opsin as the photopigment in the slit eyes and another as a putative photoisomerase found in photoreceptors of all four eyes types. The last antibody stained nerve-like cells in the tentacles, in connection with nematocytes, and the radial nerve, in connection with the gonads. This is the first time photopigment expression has been localized to the outer segments of the photoreceptors in a cnidarian ocellus (simple eye). The potential presence of a photoisomerase could be another interesting convergence between box jellyfish and vertebrate photoreceptors, but it awaits final experimental proof. 
    more » « less
  4. 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 λ max 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. 
    more » « less
  5. Synopsis Animals use visual communication to convey crucial information about their identity, reproductive status, and sex. Plasticity in the auditory and olfactory systems has been well-documented, however, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice are largely dependent on visual signals across taxa. We previously found reproductive state-dependent plasticity in the eye of the highly social cichlid fish Astatotilapia burtoni. Male A. burtoni increase their courtship, including multicomponent visual displays, when around ovulated females, and ovulated females are more responsive to male visual courtship displays than non-ovulated females. Based on this, we hypothesized that ovulation status impacts visual capabilities in A. burtoni females. Using electroretinograms, we found that ovulated females had greater visual sensitivity at wavelengths corresponding to male courtship coloration compared with non-reproductively-receptive females. In addition, ovulated females had higher neural activation in the retina and higher mRNA expression levels of neuromodulatory receptors (e.g., sex-steroids; gonadotropins) in the eye than non-ovulated females. Here, we add to this body of work by testing the hypothesis that cone opsin expression changes with female reproductive state. Ovulated females had higher expression of short wavelength sensitive opsins (sws1, sws2a, sws2b) compared with mouthbrooding females. Further, expression of sws2a, the most abundant opsin in the A. burtoni eye, positively correlated with levels of circulating 11-ketotestosterone and estradiol and estrogen, androgen, and gonadotropin system receptor expression in the eye in females. These data indicate that reproductive state-dependent plasticity also occurs at the level of photoreceptors, not just through modulation of visual signals at downstream retinal layers. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females. 
    more » « less