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The vertebrate retina has several spectral types of cone photoreceptor. Each photo-receptor contains a visual pigment that is maximally sensitive to ultraviolet (UV), blue, green or red light1and consists of a protein (opsin) attached to a chromophore (a derivative of vitamin A1 or vitamin A2)1. It is the combined input from cones containing different visual pigments, each with a different spectral phenotype, that allows an animal to perceive colour.

Changes in colour sensitivity in the outer retina arise from altering the density of different cone types2 or by switching chromophores (vitamin A2-based visual pigments absorb light of longer wavelengths than their vitamin A1 counterparts)3. Another way to modulate colour vision would be to switch between different opsins, a mechanism that we investigate here in the cone photo-receptors of the Pacific pink salmon.

To determine whether it is possible for such a phenotypic transformation to occur: we measured the absorbance of visual pigment along the outer segment of individual cones by using microspectrophotometry3 (the outer segment of a cone consists of stacked lipid bilayers that contain the visual pigment)1; we also labelled opsin messenger RNAs by using in situ hybridization4 with salmon-specific molecular probes.

We found that all the single cones in recently hatched fish (weight about 0.4 g) contain a visual pigment with maximum absorbance in the ultraviolet (λmax of the visual pigment: 365–375 nm); however, as the fish grew (weight exceeding 0.8 g), the single cones stopped producing UV-opsin and started to produce blue-opsin (λmax of the visual pigment: 425–435 nm) in a transformation event that proceeds from the ventral to the dorsal retina.

When absorbance is measured from the tip to the base of a cone outer segment undergoing such a transformation, the absorbance is ultraviolet-dominated at the tip, becoming blue-dominated at the base (Fig. 1a). As the outer-segment bilayers are produced at the base and removed from the tip5, these results show that the UV-opsin is being replaced by blue-opsin during the transformation.

Figure 1: Absorbance measurements and double in situ labelling of single cones in Pacific pink salmon with ultraviolet- and blue-opsin riboprobes.
figure 1

a, Cones show increased absorbance in the ultraviolet at the tip of the outer segment (right) and increased absorbance of blue light at the base, with intermediate absorbances in between (traces are composite averages from seven cones). b, Tangential retinal section showing single cones labelled by in situ hybridization with probes specific for mRNAs encoding UV-opsin (shown in blue) or blue-opsin (in red); cones coexpressing both mRNAs appear purple (arrows). c,d, Single cones are labelled with only the UV-opsin riboprobe before the switch in opsin expression (c), and with only the blue-opsin riboprobe afterwards (d). Scale bars: b, 5.5 µm; c, 7.8 µm; and d, 13 µm.

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In agreement with this finding, fish in the process of transformation have a mixture of ultraviolet- and blue-sensitive cones, with some cones expressing both opsins together (Fig. 1b). Before the transformation, single cones express only UV-opsin (Fig. 1c); afterwards, they express only blue-opsin (Fig. 1d). Salmonid fish also lose some single (corner) cones following this transformation2, further reducing their ultraviolet/blue sensitivity.

This opsin switch in the single cones of pink salmon represents a previously undiscovered way to modulate colour vision. The transformation is linked to a progressive change in the lifestyle of the salmon6, which starts as a planktivore in surface waters, where ultraviolet light is abundant, and becomes a fish-eating predator in deeper waters, where blue-green light prevails. As several other vertebrates are known to co-express different opsins in a cone7,8,9,10, such a mechanism for temporal modulation of colour vision may be widespread.