Abstract
We examined neuronal responses of hypothalamic melanin-concentrating hormone (MCH) and corticotropin-releasing hormone (CRH) to background color in the self-fertilizing fish, Kryptolebias marmoratus. Fish were individually reared in lidless white or black cylindrical plastic containers for 15 days. The number of MCH-immunoreactive (ir) cell bodies in the nucleus lateralis tuberis (NLT) of the hypothalamus was significantly greater in the white-acclimated fish, while no significant differences were observed in the nucleus anterior tuberis (NAT) of the hypothalamus. Significant differences were not seen in the number of CRH-ir cell bodies in the NLT between the groups. The body of the white- and black-acclimated fish appeared lighter and darker, respectively, compared with the baseline color. In the black-acclimated fish, feeding activity was significantly greater with a tendency toward higher specific growth rate compared with the observations in white-acclimated fish. No significant inter-group cortisol level differences were observed. These results indicate that background color affects MCH neuronal activity in the NLT as well as body color adaptation but does not affect CRH neuronal activity in K. marmoratus.
Similar content being viewed by others
Data availability
The datasets and materials used during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
Abbreviations
- C:
-
Cerebellum
- CP:
-
Central posterior thalamic nucleus
- GA:
-
Corpus glomerulosus pars anterior
- GR:
-
Corpus glomerulosus pars rotunda
- HB:
-
Habenula
- Hyp:
-
Hypothalamus
- LI:
-
Inferior lobe
- M:
-
Medulla oblongata
- NAT:
-
Nucleus anterior tuberis
- NC:
-
Nucleus corticalis
- NLT:
-
Nucleus lateralis tuberis
- NRL:
-
Nucleus recessi lateralis
- OB:
-
Olfactory bulb
- OT:
-
Optic tectum
- PG:
-
Preglomerular complex
- PGZ:
-
Periventricular gray zone of optic tectum
- Pit:
-
Pituitary
- T:
-
Telencephalon
- TE:
-
Tectum
- TL:
-
Torus longitudinalis
- TLa:
-
Torus lateralis
- TS:
-
Torus semicircularis
- VM:
-
Ventromedial thalamic nucleus
References
Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247. https://doi.org/10.1002/ar.1090940210
Amano M, Takahashi A (2009) Melanin-concentrating hormone: A neuropeptide hormone affecting the relationship between photic environment and fish with special reference to background color and food intake regulation. Peptides 30:1979–1984. https://doi.org/10.1016/j.peptides.2009.05.022
Amano M, Amiya N, Yokoyama T, Onikubo K, Yamamoto N, Takahashi A (2016) Immunohistochemical detection of corticotropin-releasing hormone (CRH) in the brain and pituitary of the hagfish, Eptatretus burgeri. Gen Comp Endocrinol 236:174–180. https://doi.org/10.1016/j.ygcen.2016.07.018
Amano M, Amiya N, Mizusawa K, Chiba H (2021) Effects of background color and rearing density on stress-related hormones in the juvenile Japanese eel Anguilla japonica. Fish Sci 87:521–528. https://doi.org/10.1007/s12562-021-01527-4
Amano M, Amiya N, Fukushima K, Hagio H, Yamamoto N, Sakakura Y (2022) Effects of crowding stress on the hypothalamo-pituitary-interrenal axis of the self-fertilizing fish Kryptolebias marmoratus. Comp Biochem Physiol A 264:111110. https://doi.org/10.1016/j.cbpa.2021.111110
Avise JC, Tatarenkov A (2015) Population genetics and evolution of the mangrove rivulus Kryptolebias marmoratus, the world’s only self-fertilizing hermaphroditic vertebrate. J Fish Biol 87:519–538. https://doi.org/10.1111/jfb.12741
Baker BI (1994) Melanin-concentrating hormone updated functional considerations. Trends Endocrinol Metab 5:120–126. https://doi.org/10.1016/1043-2760(94)90093-0
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integ Comp Biol 42:517–525. https://doi.org/10.1093/icb/42.3.517
Bird DJ, Baker BI (1989) An immunological study of the secretory activity of neurons producing melanin-concentrating hormone in a teleost. Neuroscience 28:245–251. https://doi.org/10.1016/0306-4522(89)90248-0
Cánepa MM, Pandolfi M, Maggese MC, Vissio PG (2006) Involvement of somatolactin in background adaptation of the cichlid fish Cichlasoma dimerus. J Exp Zool 305A:410–419. https://doi.org/10.1002/jez.a.273
Cerdá-Reverter JM, Canosa LF, Peter RE (2006) Regulation of the hypothalamic melanin-concentrating hormone neurons by sex steroids in the goldfish: possible role in the modulation of luteinizing hormone secretion. Neuroendocrinol 84:364–377. https://doi.org/10.1159/000098334
Costa DC, Mattioli CC, Silva WS, Takata R, Leme FOP, Oliveira AL, Luz RK (2017) The effect of environmental colour on the growth, metabolism, physiology and skin pigmentation of the carnivorous freshwater catfish Lophiosilurus alexandri. J Fish Biol 90:922–935. https://doi.org/10.1111/jfb.13208
Diniz GB, Bittencourt JC (2019) The melanin-concentrating hormone (MCH) system: a tale of two peptides. Front Neurosci 13:1280. https://doi.org/10.3389/fnins.2019.01280
Eslamloo K, Akhavan SR, Eslamifar A, Henry MA (2015) Effects of background colour on growth performance, skin pigmentation, physiological condition and innate immune responses of goldfish, Carassius auratus. Aqua Res 46:202–215. https://doi.org/10.1111/are.12177
Green JA, Baker BI, Kawauchi H (1991) The effect of rearing rainbow trout on black or white backgrounds on their secretion of melanin-concentrating hormones and their sensitivity to stress. J Endocrinol 128:267–274. https://doi.org/10.1677/joe.0.1280267
Gröneveld D, Balm PHM, Martens GJM, Bonga SEW (1995) Differential melanin-concentrating hormone gene expression in two hypothalamic nuclei of the teleost tilapia in response to environmental changes. J Neuroendocrinol 7:527–533. https://doi.org/10.1111/j.1365-2826.1995.tb00789.x
Harrington RW Jr (1961) Oviparous hermaphroditic fish with internal self-fertilization. Science 134:1749–1750. https://doi.org/10.1126/science.134.3492.1749
Kanamori A, Sugita Y, Yuasa Y, Suzuki T, Kawamura K, Uno Y, Kamimura K, Matsuda Y, Wilson CA, Amores A, Postlethwait JH, Suga K, Sakakura Y (2016) A genetic map for the only self-fertilizing vertebrate. G3 Genes Genomes Genetics 6:1095–1106. https://doi.org/10.1534/g3.115.022699
Kang D-Y, Kim H-C (2013) Influence of density and background color to stress response, appetite, growth, and blind-side hypermelanosis of flounder, Paralichthys olivaceus. Fish Physiol Biochem 39:221–232. https://doi.org/10.1007/s10696-012-9693-2
Kawauchi H, Kawazoe I, Tsubokawa M, Kishida M, Baker BI (1983) Characterization of melanin-concentrating hormone in chum salmon pituitaries. Nature 305:321–323. https://doi.org/10.1038/305321a0
Matsuda K, Shimakura SI, Maruyama K, Miura T, Uchiyama M, Kawauchi H, Shioda S, Takahashi A (2006) Central administration of melanin-concentrating hormone (MCH) suppresses food intake, but not locomotor activity, in the goldfish, Carassius auratus. Neurosci Lett 399:259–263. https://doi.org/10.1016/j.neulet.2006.02.005
Matsuda K, Shimakura SI, Miura T, Maruyama K, Uchiyama M, Kawauchi H, Shioda S, Takahashi A (2007) Feeding-induced changes of melanin-concentrating hormone (MCH)-like immunoreactivity in goldfish brain. Cell Tissue Res 328:375–382. https://doi.org/10.1007/s00441-006-0347-5
Pankhurst NW (2011) The endocrinology of stress in fish: an environmental perspective. Gen Comp Endocrinol 170:265–275. https://doi.org/10.1016/j.ygcen.2010.07.017
Peter RE, Gill VE (1975) A stereotaxic atlas and technique for forebrain nuclei in the goldfish, Carassius auratus. J Comp Neurol 159:69–102. https://doi.org/10.1002/cne.901590106
Pottinger TG, Carrick TR, Yeomans WE (2002) The three-spined stickleback as an environmental sentinel: effects of stressors on whole-body physiological indices. J Fish Biol 61:207–229. https://doi.org/10.1006/jfbi.2002.2034
Suzuki M, Narnaware YK, Baker BI, Levy A (1995) Influence of environmental colour and diurnal phase on MCH gene expression in the trout. J Neuroendocrinol 7:319–328. https://doi.org/10.1111/j.1365-2826.1995.tb00764.x
Takahashi A, Tsuchiya K, Yamanome T, Amano M, Yasuda A, Yamamori K, Kawauchi H (2004) Possible involvement of melanin-concentrating hormone in food intake in a teleost, barfin flounder. Peptides 25:1613–1622. https://doi.org/10.1016/j.peptides.2004.02.022
Takahashi A, Kosugi T, Kobayashi Y, Yamanome T, Schiöth BH, Kawauchi H (2007) The melanin-concentrating hormone receptor 2 (MCH-R2) mediates the effect of MCH to control body color for background adaptation in the barfin flounder. Gen Comp Endocrinol 151:210–219. https://doi.org/10.1016/j.ygcen.2007.01.011
Taylor DS (2012) Twenty-four years in the mud: what have we learned about the natural history and ecology of the mangrove rivulus, Kryptolebias marmoratus? Integr Comp Biol 52:724–736. https://doi.org/10.1093/icb/ics062
Wullimann MF, Rupp B, Reichert H (1996) Neuroanatomy of the zebrafish brain: a topological atlas. Birkhӓuser Verlag, Basel, Switzerland
Yamada H, Satoh R, Fujimoto Y, Takaji K, Hakuba T, Chiba H, Iwata M (2002) Circadian changes in serum concentrations of steroids in Japanese char Salvelinus leucomaenis at the stage of final maturation. Zool Sci 19:891–898. https://doi.org/10.2108/zsj.19.891
Yamanome T, Chiba H, Takahashi A (2007) Melanocyte-stimulating hormone facilitates hypermelanosis on blind side of barfin flounder, a pleuronectiform fish. Aquaculture 270:505–511. https://doi.org/10.1016/j.aquaculture.2007.05.037
Acknowledgements
We thank Ms. Ayae Kuriu, Mr. Aoi Kato, and Mr. Takashi Sato of the School of Marine Biosciences, Kitasato University, for their help in this study.
Funding
This study was supported in part by JSPS KAKENHI Grant Number JP23380115.
Author information
Authors and Affiliations
Contributions
Masafumi Amano and Yoshitaka Sakakura designed the study; Masafumi Amano, Noriko Amiya, and Naoyuki Yamamoto conducted immunohistochemistry; Naoyuki Yamamoto drew the brain atlas; Masafumi Amano and Yoshitaka Sakakura conducted the rearing experiment; Masafumi Amano drafted the manuscript and all authors approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethics approval
Fish maintenance and sacrifice were performed following the guidelines of the animal care committee of Nagasaki University and Kitasato University.
Conflict of interest
The authors declare no conflict of interest.
Consent to participate
Not applicable.
Consent to publication
Not applicable.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Amano, M., Amiya, N., Yamamoto, N. et al. Neuronal responses of melanin-concentrating hormone and corticotropin-releasing hormone to background color in the self-fertilizing fish, Kryptolebias marmoratus. Fish Physiol Biochem 49, 385–398 (2023). https://doi.org/10.1007/s10695-023-01178-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-023-01178-5