Electrophysiological assessment of spectral sensitivity in adult Nile tilapia Oreochromis niloticus: evidence for violet sensitivity

Abstract

SUMMARYThe cichlid fish radiations of the African Great Lakes are an important model for evolutionary biology. Cichlids have diverse colour vision systems and predominately express three cone visual pigments. However, rare populations of spectrally distinct cones have been found in a number of species, but it is not known whether they contribute to spectral sensitivity. Adult Nile tilapia, Oreochromis niloticus, an ancestral outgroup to the cichlid radiations in the Great Lakes, have three cone types: shortwavelength sensitive (SWS), medium-wavelength sensitive (MWS) and long-wavelength sensitive (LWS) cones, but evidence from microspectrophotometry and cone opsin gene expression suggests they may also have violet-sensitive (VS) cones. We used electrophysiology to assess spectral sensitivity in this species and found evidence of four sensitivity peaks in the ranges 380-420, 440-480, 500-600 and 600-680 nm, with maximal sensitivity at longer wavelengths. The continued presence of a 380-420 nm peak under long-wavelength chromatic adapting backgrounds indicates that this is due to a VS cone mechanism not the b-band of the LWS cone mechanism. Differences in spectral sensitivity curves recorded at different times of year revealed evidence of A1/A2 shifts. The presence of notches in the sensitivity curves and a multiple-mechanisms model used to assess cone contributions indicated that the curves are the result of four cone mechanisms (VS, SWS, MWS and LWS cones) and that chromatically opponent processes occur between mechanisms. The spectral transmittance of the lens steeply declines between 410-380 nm, limiting the short-wavelength limb of the VS cone. As adults, Nile tilapia appear to possess the necessary retinal mechanisms for colour vision. While maximal sensitivity to longer wavelengths is an adaptation to the wavelengths of light predominantly available in their natural habitats, their broad sensitivity range suggests that Nile tilapia possess a flexible, generalised visual system able to adapt to changes in visual environment in their highly variable natural habitat.

Modulation of environmental light alters reception and production of visual signals in Nile tilapia

“…This may indicate limitations of the fitting procedure rather than the lack of the VS visual pigment, as spectral sensitivity in T1 and T2 did show some short-wavelength sensitivity unaccounted for by the absorbance templates (Fig.5). Additionally, the discrepancy between our study that of Lisney et al (Lisney et al, 2010) might be a consequence of differences in background illumination used in ERG recordings, or the method used for the estimation of sensitivity. It is possible that these methodological differences obscured the sensitivity peak of the VS visual pigment concerned in the current study.…”

“…The spectral transmission of the fish lens was measured following a protocol described elsewhere (Lisney et al, 2010;Sabbah et al, 2012). Lenses were surgically removed following the completion of ERG recordings and mounted inside a cuvette.…”

“…This difference in short wavelength sensitivity was probably a result of variation in the contribution of the SWS2a pigment to spectral sensitivity (Table2 and Fig.4C,E); however, the mechanism The Journal of Experimental Biology 216 (16) underlying this modulation of spectral sensitivity between the two pairs of tanks is currently unknown. Note that, in addition to fitting the absorbance templates of the three visual pigments reported in adult Nile tilapia, we also attempted to fit the VS visual pigment identified by Lisney et al (Lisney et al, 2010); however, the resultant fit was very poor (not presented). This may indicate limitations of the fitting procedure rather than the lack of the VS visual pigment, as spectral sensitivity in T1 and T2 did show some short-wavelength sensitivity unaccounted for by the absorbance templates (Fig.5).…”

“…Juveniles predominantly express SWS2b, SWS2a, Rh2a (a combination of Rh2aβ and Rh2aα, as their maximum absorbance wavelengths, λ max , substantially overlap) and LWS (Carleton et al, 2008). Adults predominantly express SWS2a, Rh2a and LWS (Carleton et al, 2008), although evidence for a fourth, violet-sensitive (VS) visual pigment (380-420nm) has also been reported (Lisney et al, 2010). Additionally, Nile tilapia possess dermal chromatophores, thought to be composed of opsin-based light-sensitive pigments (Ban et al, 2005), suggesting that Nile tilapia may have the ability to alter body colouration independently of the visual system.…”

Functional characterisation of the chromatically antagonistic photosensitive mechanism of erythrophores in the tilapiaOreochromis niloticus

“…Previous studies in visual systems have shown that chromatic adaptation selectively depresses photosensitivity of a particular photopigment and leaves the remaining cone mechanism with prominent sensitivity (Hawryshyn and Beauchamp, 1985; Hawryshyn, 1991; Lisney et al, 2010). Here, constant UV and yellow backgrounds were used to selectively depress two candidate photopigments sensitive to UV and middle wavelengths, SWS1 and RH2b, which were possibly responsible for erythrophore aggregations and dispersions, respectively.…”