Reduced opsin gene expression in a cave-dwelling fish

Regressive evolution of structures associated with vision in cave-dwelling organisms is the focus of intense research. Most work has focused on differences between extreme visual phenotypes: sighted, surface animals and their completely blind, cave-dwelling counterparts. We suggest that troglodytic systems, comprising multiple populations that vary along a gradient of visual function, may prove critical in understanding the mechanisms underlying initial regression in visual pathways. Gene expression assays of natural and laboratory-reared populations of the Atlantic molly ( Poecilia mexicana ) revealed reduced opsin expression in cave-dwelling populations compared with surface-dwelling conspecifics. Our results suggest that the reduction in opsin expression in cave-dwelling populations is not phenotypically plastic but reflects a hardwired system not rescued by exposure to light during retinal ontogeny. Changes in opsin gene expression may consequently represent a first evolutionary step in the regression of eyes in cave organisms.

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Erratum: Temporal and spatial patterns of opsin gene expression in the zebrafish (Danio rerio): Corrections with additions

Visual Neuroscience ◽

10.1017/s0952523899163181 ◽

1999 ◽

Vol 16 (3) ◽

pp. 601-605 ◽

Cited By ~ 16

Author(s):

ELLEN A. SCHMITT ◽

GEORGE A. HYATT ◽

JOHN E. DOWLING

Keyword(s):

Gene Expression ◽

Danio Rerio ◽

Developmental Expression ◽

Opsin Gene ◽

Morphological Development ◽

Opsin Expression ◽

Temporal And Spatial Patterns ◽

Cone Opsin ◽

Temporal And Spatial ◽

Cone Opsins

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.

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Developmental and environmental plasticity in opsin gene expression in Lake Victoria cichlid fish

10.1101/2021.09.01.458542 ◽

2021 ◽

Author(s):

Lucia Irazábal-González ◽

Daniel Shane Wright ◽

Martine Maan

Keyword(s):

Gene Expression ◽

Visual System ◽

Developmental Stages ◽

Lake Victoria ◽

Developmental Trajectories ◽

Expression Profiles ◽

Cichlid Fish ◽

Opsin Gene ◽

Opsin Expression ◽

Visual Conditions

AbstractIn many organisms, sensory abilities develop and evolve according to the changing demands of navigating, foraging and communication across different environments and life stages. Teleost fish inhabit heterogeneous light environments and exhibit a large diversity in visual system properties among species. Cichlids are a classic example of this diversity, generated by different tuning mechanisms that involve both genetic factors and phenotypic plasticity. Here, we document the developmental progression of visual pigment gene expression in Lake Victoria cichlids and test if these patterns are influenced by variation in light conditions. We reared two sister species of Pundamilia to adulthood in two distinct visual conditions that resemble the two light environments that they naturally inhabit in Lake Victoria. We also included interspecific first-generation hybrids. We then quantified (using RT-qPCR) the expression of the four Pundamilia opsins (SWS2B, SWS2A, RH2A and LWS) at 14 time points. We find that opsin expression profiles progress from shorter-wavelength sensitive opsins to longer-wavelength sensitive opsins with increasing age, in both species and their hybrids. The developmental trajectories of opsin expression also responded plastically to the visual conditions. Finally, we found subtle differences between reciprocal hybrids, possibly indicating parental effects and warranting further investigation. Developmental and environmental plasticity in opsin expression may provide an important stepping stone in the evolution of cichlid visual system diversity.Research highlightsIn Lake Victoria cichlid fish, expression levels of opsin genes (encoding visual pigments) differ between developmental stages and between experimental light treatments. This plasticity may contribute to the evolution of cichlid visual system diversity.

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Spatio-temporal characterization of retinal opsin gene expression during thyroid hormone-induced and natural development of rainbow trout

Visual Neuroscience ◽

10.1017/s0952523806232139 ◽

2006 ◽

Vol 23 (2) ◽

pp. 169-179 ◽

Cited By ~ 19

Author(s):

KATHY VELDHOEN ◽

W. TED ALLISON ◽

NIK VELDHOEN ◽

BRADLEY R. ANHOLT ◽

CAREN C. HELBING ◽

...

Keyword(s):

Gene Expression ◽

Rainbow Trout ◽

Thyroid Hormone ◽

Mrna Expression ◽

Opsin Gene ◽

Control Fish ◽

Mrna Levels ◽

Cone Photoreceptors ◽

Opsin Expression ◽

Natural Development

The abundance and spatial distribution of retinal cone photoreceptors change during thyroid hormone (TH)-induced and natural development of rainbow trout (Oncorhynchus mykiss). These changes are thought to allow the fish to adapt to different photic environments throughout its life history. To date, the ontogeny of rainbow trout cone photoreceptors has been examined using physiological and morphological approaches. In this study, we extended these observations by measuring opsin gene expression in retinal quadrants during natural and TH-induced development. Gene expression during natural development was investigated in retinae from fish at both parr and smolt stages. The role of TH in modulating opsin gene expression was determined in TH-treated parr and control fish sampled after two, nine, and 22 days of treatment. Total RNA was isolated from each retinal quadrant and steady-state opsin mRNA levels were measured using reverse transcriptase real-time quantitative polymerase chain reaction (QPCR) analysis. Expression of ultraviolet-sensitive opsin (SWS1), rod opsin (RH1), middle wavelength-sensitive opsin (RH2), and long wavelength-sensitive opsin (LWS) transcripts vary spatially in the parr retina. Smolts, compared to parr, had downregulated SWS1 expression in all quadrants, lower LWS expression dorsally, higher RH1 expression nasally, and higher RH2 expression dorsally. In TH-treated parr, SWS1 opsin expression was downregulated in the nasal quadrants by two days. SWS1 displayed the greatest degree of downregulation in all quadrants after nine days of treatment, with an increase in short wavelength-sensitive (SWS2) and RH2 opsin mRNA expression in the temporal quadrants. This study reveals that opsin genes display spatially significant differences within rainbow trout retina in their level of mRNA expression, and that regulation of opsin expression is a dynamic process that is influenced by TH. This is particularly evident for SWS1 gene expression in parr following TH-induced and natural development.

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Intra-retinal variation of opsin gene expression in the guppy (Poecilia reticulata)

Journal of Experimental Biology ◽

10.1242/jeb.057836 ◽

2011 ◽

Vol 214 (19) ◽

pp. 3248-3254 ◽

Cited By ~ 16

Author(s):

D. J. Rennison ◽

G. L. Owens ◽

W. T. Allison ◽

J. S. Taylor

Keyword(s):

Gene Expression ◽

Poecilia Reticulata ◽

Opsin Gene

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A hypomorphic cystathionine ß-synthase gene contributes to cavefish eye loss by disrupting optic vasculature

Nature Communications ◽

10.1038/s41467-020-16497-x ◽

2020 ◽

Vol 11 (1) ◽

Cited By ~ 1

Author(s):

Li Ma ◽

Aniket V. Gore ◽

Daniel Castranova ◽

Janet Shi ◽

Mandy Ng ◽

...

Keyword(s):

Circulatory System ◽

Astyanax Mexicanus ◽

Transsulfuration Pathway ◽

Key Enzyme ◽

Surface Dwelling ◽

Blind Cave ◽

Vestigial Structures ◽

Key Indicators ◽

Evolutionary Descent ◽

Eye Formation

Abstract Vestigial structures are key indicators of evolutionary descent, but the mechanisms underlying their development are poorly understood. This study examines vestigial eye formation in the teleost Astyanax mexicanus, which consists of a sighted surface-dwelling morph and multiple populations of blind cave morphs. Cavefish embryos initially develop eyes, but they subsequently degenerate and become vestigial structures embedded in the head. The mutated genes involved in cavefish vestigial eye formation have not been characterized. Here we identify cystathionine ß-synthase a (cbsa), which encodes the key enzyme of the transsulfuration pathway, as one of the mutated genes responsible for eye degeneration in multiple cavefish populations. The inactivation of cbsa affects eye development by increasing the transsulfuration intermediate homocysteine and inducing defects in optic vasculature, which result in aneurysms and eye hemorrhages. Our findings suggest that localized modifications in the circulatory system may have contributed to the evolution of vestigial eyes in cavefish.

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Ontogenetic changes in photoreceptor opsin gene expression in coho salmon (Oncorhynchus kisutch, Walbaum)

Journal of Experimental Biology ◽

10.1242/jeb.020289 ◽

2008 ◽

Vol 211 (24) ◽

pp. 3879-3888 ◽

Cited By ~ 30

Author(s):

S. E. Temple ◽

K. M. Veldhoen ◽

J. T. Phelan ◽

N. J. Veldhoen ◽

C. W. Hawryshyn

Keyword(s):

Gene Expression ◽

Coho Salmon ◽

Oncorhynchus Kisutch ◽

Opsin Gene ◽

Ontogenetic Changes

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Behavioural, physiological and metabolic responses to long-term starvation and refeeding in a blind cave-dwelling (Proteus anguinus) and a surface-dwelling (Euproctus asper) salamander

Journal of Experimental Biology ◽

10.1242/jeb.204.2.269 ◽

2001 ◽

Vol 204 (2) ◽

pp. 269-281 ◽

Cited By ~ 2

Author(s):

F. Hervant ◽

J. Mathieu ◽

J. Durand

Keyword(s):

Food Deprivation ◽

Metabolic Response ◽

Energy System ◽

Energy Reserves ◽

Energy Strategy ◽

Quick Recovery ◽

Proteus Anguinus ◽

Surface Dwelling ◽

Blind Cave

The effects of long-term starvation and subsequent refeeding on haematological variables, behaviour, rates of oxygen consumption and intermediary and energy metabolism were studied in morphologically similar surface- and cave-dwelling salamanders. To provide a hypothetical general model representing the responses of amphibians to food stress, a sequential energy strategy has been proposed, suggesting that four successive phases (termed stress, transition, adaptation and recovery) can be distinguished. The metabolic response to prolonged food deprivation was monophasic in the epigean Euproctus asper (Salamandridae), showing an immediate, linear and large decrease in all the energy reserves. In contrast, the hypogean Proteus anguinus (Proteidae) displayed successive periods of glucidic, lipidic and finally lipido-proteic-dominant catabolism during the course of food deprivation. The remarkable resistance to long-term fasting and the very quick recovery from nutritional stress of this cave organism may be explained partly by its ability to remain in an extremely prolonged state of protein sparing and temporary torpor. Proteus anguinus had reduced metabolic and activity rates (considerably lower than those of most surface-dwelling amphibians). These results are interpreted as adaptations to a subterranean existence in which poor and discontinuous food supplies and/or intermittent hypoxia may occur for long periods. Therefore, P. anguinus appears to be a good example of a low-energy-system vertebrate.

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Modeling binary and graded cone cell fate patterning in the mouse retina

10.1101/650606 ◽

2019 ◽

Author(s):

Kiara C. Eldred ◽

Cameron Avelis ◽

Robert J. Johnston ◽

Elijah Roberts

Keyword(s):

Gene Expression ◽

Thyroid Hormone ◽

Cell Fate ◽

Regulatory Network ◽

Photoreceptor Cells ◽

Mouse Retina ◽

Hormone Signaling ◽

Cell Fates ◽

Opsin Expression ◽

A Cell

AbstractNervous systems are incredibly diverse, with myriad neuronal subtypes defined by gene expression. How binary and graded fate characteristics are patterned across tissues is poorly understood. Expression of opsin photopigments in the cone photoreceptors of the mouse retina provides an excellent model to address this question. Individual cones express S-opsin only, M-opsin, or both S-opsin and M-opsin. These cell populations are patterned along the dorsal-ventral axis, with greater M-opsin expression in the dorsal region and greater S-opsin expression in the ventral region. Thyroid hormone signaling plays a critical role in activating M-opsin and repressing S-opsin. Here, we developed an image analysis approach to identify individual cone cells and evaluate their opsin expression from immunofluorescence imaging tiles spanning roughly 6 mm along the D-V axis of the mouse retina. From analyzing the opsin expression of ∼250,000 cells, we found that cones make a binary decision between S-opsin only and co-expression competent fates. Co-expression competent cells express graded levels of S- and M-opsins, depending nonlinearly on their position in the dorsal-ventral axis. M- and S-opsin expression display differential, inverse patterns. Using these single-cell data we developed a quantitative, stochastic model of cone cell decisions in the retinal tissue based on thyroid hormone signaling activity. The model recovers the probability distribution for cone fate patterning in the mouse retina and describes a minimal set of interactions that are necessary to reproduce the observed cell fates. Our study provides a paradigm describing how differential responses to regulatory inputs generate complex patterns of binary and graded cell fates.Author SummaryThe development of a cell in a mammalian tissue is governed by a complex regulatory network that responds to many input signals to give the cell a distinct identity, a process referred to as cell-fate specification. Some of these cell fates have binary on-or-off gene expression patterns, while others have graded gene expression that changes across the tissue. Differentiation of the photoreceptor cells that sense light in the mouse retina provides a good example of this process. Here, we explore how complex patterns of cell fates are specified in the mouse retina by building a computational model based on analysis of a large number of photoreceptor cells from microscopy images of whole retinas. We use the data and the model to study what exactly it means for a cell to have a binary or graded cell fate and how these cell fates can be distinguished from each other. Our study shows how tens-of-thousands of individual photoreceptor cells can be patterned across a complex tissue by a regulatory network, creating a different outcome depending upon the received inputs.

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