Taisho-Sanshoku koi have hardly faded skin and show attenuated melanophore sensitivity to adrenaline and melanin-concentrating hormone

Abstract

Introduction: Koi carp, an ornamental fish derived from the common carp Cyprinus carpio (CC), is characterized by beautiful skin color patterns. However, the mechanism that gives rise to the characteristic vivid skin coloration of koi carp has not been clarified. The skin coloration of many teleosts changes in response to differences in the background color. This change in skin coloration is caused by diffusion or aggregation of pigment granules in chromatophores and is regulated mainly by sympathetic nerves and hormones. We hypothesized that there would be some abnormality in the mechanism of skin color regulation in koi carp, which impairs skin color fading in response to background color.

Methods: We compared the function of melanin-concentrating hormone (MCH), noradrenaline, and adrenaline in CC and Taisho-Sanshoku (TS), a variety of tri-colored koi.

Results and discussion: In CC acclimated to a white background, the skin color became paler and pigment granules aggregated in melanophores in the scales compared to that in black-acclimated CC. There were no clear differences in skin color or pigment granule aggregation in white- or black-acclimated TS. The expression of mch1 mRNA in the brain was higher in the white-acclimated CC than that in the black-acclimated CC. However, the expression of mch1 mRNA in the brain in the TS did not change in response to the background color. Additionally, plasma MCH levels did not differ between white- and black-acclimated fish in either CC or TS. In vitro experiments showed that noradrenaline induced pigment aggregation in scale melanophores in both CC and TS, whereas adrenaline induced pigment aggregation in the CC but not in the TS. In vitro administration of MCH induced pigment granule aggregation in the CC but not in the TS. However, intraperitoneal injection of MCH resulted in pigment granule aggregation in both CC and TS. Collectively, these results suggest that the weak sensitivity of scale melanophores to MCH and adrenaline might be responsible for the lack of skin color change in response to background color in the TS.

Keywords: background color; catecholamine; koi carp; melanin-concentrating hormone; melanophore; skin color.

Figure 1

Effects of background color on skin color. Initial (upper) and final (lower) images of the dorsal skin of representative fish in 3 day- or 3 week-experiment. CCb, black-acclimated common carp; CCw, white-acclimated common carp; TSb, black-acclimated Taisho-Sanshoku; TSw, white-acclimated Taisho-Sanshoku. Scale bar = 1 cm.

Figure 2

Effects of background color on skin color fading. Degree of skin color fading of common carp and Taisho-Sanshoku in the 3-day (A) and 3-week (B) rearing experiments. Data are shown as mean ± standard error (SE). Asterisks indicate statistically significant differences estimated using the Welch test (***P < 0.001, n = 10).

Figure 3

Effects of background color on the expression of melanin-concentrating hormone (mch) mRNA in the brain. The mRNA levels of mch1, mch2a, and mch2b in the brain in the 3-day (A, C, E) and 3-week rearing experiments (B, D, F). Data are shown as mean ± SE. Asterisk indicates statistically significant difference estimated using the Welch test (*P < 0.05, n = 10).

Figure 4

Effects of background color on plasma MCH level. Plasma MCH levels in the 3-day rearing experiment (A) and 3-week rearing experiment (B). Data are shown as mean ± SE. No significant difference was estimated using the Welch test; n = 10 for CCb and CCw n = 5 for TSb, and n = 6 for TSw.

Figure 5

In vitro and ex vivo pigment-aggregating effects of MCH. Extent of melanosome area in the scales of CC (A, B) and TS (C, D) injected intraperitoneally with MCH (A, C) or treated with MCH ex vivo (B, D). Data are shown as mean ± SE. Different letters indicate statistically significant differences estimated by one-way analysis of variance (ANOVA) followed by Tukey’s honestly significant difference (HSD) test; P < 0.05, n = 6 for (A) and (C), n = 3 for (B) and (D).

Figure 6

In vitro pigment-aggregating effects of noradrenaline and adrenaline. Degree of melanosome dispersion in the scales of CC (A, C) and TS (B, D) treated ex vivo with noradrenaline (A, B) or adrenaline (C, D). Data are shown as mean ± SE.Different letters indicate statistically significant differences estimated by one-way ANOVA followed by Tukey’s HSD test; P < 0.05, n = 6.

Figure 7

Expression of melanin-concentrating hormone receptor (mchr) mRNA in the scale. The mRNA levels of mchr1a (A), mchr1b (B), mchr2S (C), and mchr2L (D) in the dorsal skin of common carp (CCs) and black-, red- and white-colored dorsal skin of TS (TSbs, TSrs, and TSws, respectively). Data are shown as mean ± SE. Different letters indicate statistically significant differences estimated by ANOVA followed by Tukey’s HSD test; P < 0.05, n = 8.