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First published online June 13, 2008
Journal of Experimental Biology 211, 2134-2143 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.009365
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Effects of exogenous thyroid hormones on visual pigment composition in coho salmon (Oncorhynchus kisutch)

Shelby E. Temple1, Samuel D. Ramsden1, Theodore J. Haimberger1, Kathy M. Veldhoen1, Nik J. Veldhoen2, Nicolette L. Carter1, Wolff-Michael Roth3 and Craig W. Hawryshyn1,4,*

1 Department of Biology, University of Victoria, Victoria, British Columbia, Canada
2 Department of Microbiology and Biochemistry, University of Victoria, Victoria, British Columbia, Canada
3 Faculty of Education Research, University of Victoria, Victoria, British Columbia, Canada
4 Department of Biology and Center for Neuroscience Studies, Queen's University, Kingston, Ontario, Canada


Figure 1
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  		Fig. 1. Group mean {lambda}max ± 2 s.e.m. of rods for the control group (circles) and TH treatment group (triangles) from Experiment I performed January–March (A) and Experiment II performed in July and August (B). Each point is the mean rod {lambda}max of all coho salmon (Oncorhynchus kisutch, Walbaum) sampled at the specified time point (N values below error bars equal number of fish). The mean {lambda}max for each fish was based on the mean {lambda}max of ~20 rods measured using MSP. Treated fish received commercial salmon pellets sprayed with 12 p.p.m. T3 and 120 p.p.m. T4 by weight dissolved in ethanol. The horizontal bar shows the timing of the transition from the treatment (gray) to the control (white) diet for the treatment group. The control group remained on a diet of commercial salmon pellets sprayed with ethanol only for the duration of the experiments.

 

Figure 2
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  		Fig. 2. Group mean {lambda}max ± 2 s.e.m. of rods, middle-wavelength-sensitive (MWS) and long-wavelength-sensitive (LWS) cones from control and treatment groups for Experiments III–V (plotted in numerical order from left to right). Absorbance spectra of individual photoreceptors from the dorsal retina of coho salmon (Oncorhynchus kisutch, Walbaum) were measured using MSP. The group mean {lambda}max is based on the mean of all fish sampled for that group, and the mean {lambda}max for each fish is the mean of ~20 rods, 10 MWS or 8 LWS cones (on average). The control and TH-treated group mean {lambda}max values for rods, MWS and LWS cones were significantly different from one another (P<0.001) in all three experiments.

 

Figure 3
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  		Fig. 3. Frequency histograms of {lambda}max values for rods (A), long-wavelength-sensitive (LWS) cones (B) and middle-wavelength-sensitive (MWS) cones (C) recorded from all control and TH-treated coho salmon (Oncorhynchus kisutch, Walbaum) used in Experiments III–V.

 

Figure 4
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  		Fig. 4. Six models that predict the expected shift in visual pigment {lambda}max ({Delta}{lambda}max=A2{lambda}max–A1{lambda}max) when one opsin is combined with vitamins A1 and A2 chromophores as a function of the {lambda}max of the vitamin A1 member. These models are compared with the observed values for rods, middle-wavelength-sensitive (MWS) and long-wavelength-sensitive (LWS) cones in coho salmon (Oncorhynchus kisutch, Walbaum). Lines representing each model are from Bridges (Bridges, 1965Go) (gray dotted), from Dartnall and Lythgoe (Dartnall and Lythgoe, 1965Go) (gray dashed), from Tsin et al. (Tsin et al., 1981Go) (gray dotted and dashed), from Whitmore and Bowmaker (Whitmore and Bowmaker, 1989Go) (black dotted and dashed), from Harosi (Harosi, 1994Go) (solid black), and from Parry and Bowmaker (Parry and Bowmaker, 2000Go) (black dashed). The observed range for rods, MWS and LWS cones based on the mean per fish are plotted as filled circles. The spectral shift observed in rods and LWS cones falls within the predicted range of the models, indicating that the observed variance in {lambda}max values can be explained by a change in chromophore ratio. The spectral shift of MWS cones lies outside the range predicted by all six models and therefore the variance in {lambda}max of MWS cones cannot be explained by a shift in chromophore ratio alone: a second RH2 opsin subtype is implicated in this shift.

 

Figure 5
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  		Fig. 5. Scatter plot showing {lambda}max values for middle-wavelength-sensitive (MWS) and long-wavelength-sensitive (LWS) outer segments from individual double cones where both outer segments were measured. The horizontal dashed lines indicate the minimum and maximum {lambda}max values predicted for a single LWS opsin with a {lambda}max range of 5631–6332 nm using Harosi's (Harosi, 1994Go) model (for model selection criteria, see text). Vertical dotted line predicts the range of {lambda}max values for the MWS cones at the short-wavelength range of the data set. Vertical dotted and dashed line predicts the range of {lambda}max values based on the long-wavelength range of the data set. All data points fit between these vertical and horizontal limits within the measurement error of the MSP device (±3 nm), except those in the lower range of the LWS data set (see text). Using the lower value of 4951 nm as the vitamin A1 observed value, we used Whitmore and Bowmaker's (Whitmore and Bowmaker, 1989Go) model to calculate that the same opsin would have a {lambda}max of 5232 nm if combined with a vitamin A2 chromophore. Using the inverse of Whitmore and Bowmaker's (Whitmore and Bowmaker, 1989Go) model, we estimated that the vitamin A1-based visual pigment that corresponded to the 5482 nm MWS cone value at the long-wavelength end of the range would have a {lambda}max of 5121 nm.

 

Figure 6
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  		Fig. 6. Alignment between the amino acid sequences of the coho (Oncorhynchus kisutch, Walbaum) RH2A (Dann et al., 2004Go) and RH2B protein deduced from coho middle-wavelength-sensitive (MWS) opsin cDNA show 86.1 percent amino acid sequence identity. Conserved residues in positions analogous to bovine I113, C187 and K296 are in bold. The 48 amino acid differences between the RH2A and RH2B are marked by asterisks below the sequence. The E123Q substitution (analogous to position 122 in bovine rod opsin), which may be responsible for the short-wavelength shift of the RH2B relative to RH2A, is in bold with an asterisk below.

 

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© The Company of Biologists Ltd 2008