Possible Involvement of Cone Opsins in Distinct Photoresponses of Intrinsically Photosensitive Dermal Chromatophores in Tilapia Oreochromis niloticus

Animals often change their habitat throughout ontogeny; yet, the triggers for habitat transitions and how these correlate with developmental changes -e.g. physiological, morphological and behavioural -remain largely unknown. Here, we investigated how ontogenetic changes in body coloration and of the visual system relate to habitat transitions in a coral reef fish. Adult dusky dottybacks, Pseudochromis fuscus, are aggressive mimics that change colour to imitate various fishes in their surroundings; however, little is known about the early life stages of this fish. Using a developmental time series in combination with the examination of wild-caught specimens, we revealed that dottybacks change colour twice during development: (i) nearly translucent cryptic pelagic larvae change to a grey camouflage coloration when settling on coral reefs; and (ii) juveniles change to mimic yellow-or brown-coloured fishes when reaching a size capable of consuming juvenile fish prey. Moreover, microspectrophotometric (MSP) and quantitative real-time PCR (qRT-PCR) experiments show developmental changes of the dottyback visual system, including the use of a novel adult-specific visual gene (RH2 opsin). This gene is likely to be co-expressed with other visual pigments to form broad spectral sensitivities that cover the medium-wavelength part of the visible spectrum. Surprisingly, the visual modifications precede changes in habitat and colour, possibly because dottybacks need to first acquire the appropriate visual performance before transitioning into novel life stages.

Section: Discussionmentioning

confidence: 99%

From crypsis to mimicry: changes in colour and the configuration of the visual system during ontogenetic habitat transitions in a coral reef fish

Cortesi

Musilová

Stieb

et al. 2016

“…However, extraocular photoreceptors can also express opsins identical to those in the retina and may potentially use visual phototransductive pathways. Examples of these include rhodopsin in the light organ and parolfactory vesicles of squids and cone opsins in the dermis of fish (Hara and Hara, 1980;Tong et al, 2009;Ban et al, 2005;Kasai and Oshima, 2006;Chen et al, 2013). Nile tilapia (Oreochromis niloticus) and neon tetra (Paracheirodon innesi) are particularly notable, because opsins identical to those in the retina play a role in initiating signals that result in expansion and contraction of pigment cells (chromatophores) or modulation of the color reflected from iridophores.…”

Section: Introductionmentioning

confidence: 99%

Visual phototransduction components in cephalopod chromatophores suggest dermal photoreception

Kingston

Kuzirian

Hanlon

et al. 2015

Cephalopod mollusks are renowned for their colorful and dynamic body patterns, produced by an assemblage of skin components that interact with light. These may include iridophores, leucophores, chromatophores and (in some species) photophores. Here, we present molecular evidence suggesting that cephalopod chromatophores -small dermal pigmentary organs that reflect various colors of light -are photosensitive. RT-PCR revealed the presence of transcripts encoding rhodopsin and retinochrome within the retinas and skin of the squid Doryteuthis pealeii, and the cuttlefish Sepia officinalis and Sepia latimanus. In D. pealeii, G qα and squid TRP channel transcripts were present in the retina and in all dermal samples. Rhodopsin, retinochrome and G qα transcripts were also found in RNA extracts from dissociated chromatophores isolated from D. pealeii dermal tissues. Immunohistochemical staining labeled rhodopsin, retinochrome and G qα proteins in several chromatophore components, including pigment cell membranes, radial muscle fibers, and sheath cells. This is the first evidence that cephalopod dermal tissues, and specifically chromatophores, may possess the requisite combination of molecules required to respond to light.

“…neurohormones) or external stimuli (e.g. light), chromatophores are able to make rapid, remarkable colour changes (Mäthger et al, 2003;Ban et al, 2005;Chen et al, 2013;Nilsson Sköld et al, 2013). For example, intrinsically photosensitive dermal chromatophores of the Nile tilapia Oreochromis niloticus demonstrate distinct photoresponses (Chen et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…light), chromatophores are able to make rapid, remarkable colour changes (Mäthger et al, 2003;Ban et al, 2005;Chen et al, 2013;Nilsson Sköld et al, 2013). For example, intrinsically photosensitive dermal chromatophores of the Nile tilapia Oreochromis niloticus demonstrate distinct photoresponses (Chen et al, 2013). Independent of wavelength, the black pigments (melanosomes) of melanophores tend to disperse and melanophores maintain dispersion state by shuffling pigment granules (Chen et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…For example, intrinsically photosensitive dermal chromatophores of the Nile tilapia Oreochromis niloticus demonstrate distinct photoresponses (Chen et al, 2013). Independent of wavelength, the black pigments (melanosomes) of melanophores tend to disperse and melanophores maintain dispersion state by shuffling pigment granules (Chen et al, 2013). By contrast, the aggregations and dispersion of red pigment (erythrosomes) of erythrophores are induced in different spectral ranges (Ban et al, 2005;Chen et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Chen

Xiao

Troje

et al. 2015

Self Cite

Non-visual photoreceptors with diverse photopigments allow organisms to adapt to changing light conditions. Whereas visual photoreceptors are involved in image formation, non-visual photoreceptors mainly undertake various non-image-forming tasks. They form specialised photosensory systems that measure the quality and quantity of light and enable appropriate behavioural and physiological responses. Chromatophores are dermal non-visual photoreceptors directly exposed to light and they not only receive ambient photic input but also respond to it. These specialised photosensitive pigment cells enable animals to adjust body coloration to fit environments, and play an important role in mate choice, camouflage and ultraviolet (UV) protection. However, the signalling pathway underlying chromatophore photoresponses and the physiological importance of chromatophore colour change remain under-investigated. Here, we characterised the intrinsic photosensitive system of red chromatophores (erythrophores) in tilapia. Like some nonvisual photoreceptors, tilapia erythrophores showed wavelengthdependent photoresponses in two spectral regions: aggregations of inner pigment granules under UV and short-wavelengths and dispersions under middle-and long-wavelengths. The action spectra curve suggested that two primary photopigments exert opposite effects on these lightdriven processes: SWS1 (short-wavelength sensitive 1) for aggregations and RH2b (rhodopsin-like) for dispersions. Both western blot and immunohistochemistry showed SWS1 expression in integumentary tissues and erythrophores. The membrane potential of erythrophores depolarised under UV illumination, suggesting that changes in membrane potential are required for photoresponses. These results suggest that SWS1 and RH2b play key roles in mediating intrinsic erythrophore photoresponses in different spectral ranges and this chromatically dependent antagonistic photosensitive mechanism may provide an advantage to detect subtle environmental photic change.