Hormonal regulation of colour change in eyes of a cryptic fish

Abstract

Colour change of the skin in lower vertebrates such as fish has been a subject of great scientific and public interest. However, colour change also takes place in eyes of fish and while an increasing amount of data indicates its importance in behaviour, very little is known about its regulation. Here, we report that both eye and skin coloration change in response to white to black background adaptation in live sand goby Pomatoschistus minutes, a bentic marine fish. Through in vitro experiments, we show that noradrenaline and melanocyte concentrating hormone (MCH) treatments cause aggregation of pigment organelles in the eye chromatophores. Daylight had no aggregating effect. Combining forskolin to elevate intracellular cyclic adenosine monophosphate (cAMP) with MCH resulted in complete pigment dispersal and darkening of the eyes, whereas combining prolactin, adrenocorticotrophic hormone (ACTH) or melanocyte stimulating hormone (α-MSH) with MCH resulted in more yellow and red eyes. ACTH and MSH also induced dispersal in the melanophores, resulting in overall darker eyes. By comparing analysis of eyes, skin and peritoneum, we conclude that the regulation pattern is similar between these different tissues in this species which is relevant for the cryptic life strategy of this species. With the exception of ACTH which resulted in most prominent melanophore pigment dispersal in the eyes, all other treatments provided similar results between tissue types. To our knowledge, this is the first study that has directly analysed hormonal regulation of physiological colour change in eyes of fish.

Keywords: Camouflage; Erythrophores; Iris; Melanophores; Physiological colour change; Pigment.

Fig. 1.. Eye coloration in living sand goby, Pomatoschistus minutus.

(A) Photograph of a male sand goby guarding his nest. (B) Photograph of a sand goby on gravel. (C) Close-up micrograph of an eye in situ shows that the dorsal area is densely pigmented while the ventral side contains more reflective pigment. (D) Photograph taken from above the fish shows that the eye has a flat iris whereas the rest of the eye is spherical in shape and pigmented at the dorsal part. All photographs reveal cryptic eyes, similar in coloration to the rest of the head.

Fig. 2.. Background adaptation in living sand goby, Pomatoschistus minutus.

Fish kept on a white background became considerable pale throughout the body and in the eyes (A,B), whereas the same fish showed darkening of the skin and eyes after subsequent transfer to dark background (C,D). B and D are magnifications of head area in A and C, respectively.

Fig. 3.. Physiological colour change in vitro in eyes of sand goby, Pomatoschistus minutus.

Left panel are controls incubated in Ringers solution, whereas right panel is the hormone treated of the same eye pair with the results of pigment aggregation and paling of iris by MCH (A) and NA (B) after 3 h treatment. (C) The eyes were pre-incubated with MCH for 1 h to induce chromatophore pigment aggregation and then forskolin was added to one eye in the pair (right) with the results of pigment dispersal and darkening of the eye. Insert in C shows the MCH mediated paling of the eye before forskolin was added. Scale bars: 0.2 mm.

Fig. 4.. Physiological colour change in vitro in eyes of sand goby, Pomatoschistus minutus.

Pigment dispersal effects of prolactin (A), ACTH (B) and α-MSH (C) after 3 h treatment. Left panel are controls incubated in MCH in Ringers solution, whereas right panel is incubated in MCH+the putative dispersal hormone for the same eye pair. Prolactin resulted in more orange coloration only compared to MCH only, whereas ACTH and α-MSH also caused melanophore pigment dispersal resulting in darker eyes. All eyes were pre-treated in MCH for at least one hour to induce pigment aggregation before addition of the dispersal hormone. Scale bar: 0.2 mm.