Fish Physiology and Biochemistry

, Volume 44, Issue 3, pp 817–828 | Cite as

Effects of temperature and melatonin on day–night expression patterns of arginine vasotocin and isotocin mRNA in the diencephalon of a temperate wrasse Halichoeres tenuispinis

  • Selma Bouchekioua
  • Sung-Pyo Hur
  • Yuki Takeuchi
  • Young-Don Lee
  • Akihiro TakemuraEmail author


Most wrasses are protogynous species that swim to feed, reproduce during the daytime, and bury themselves under the sandy bottom at night. In temperate and subtropical wrasses, low temperature influences emergence from the sandy bottom in the morning, and induces a hibernation-like state in winter. We cloned and characterized the prohormone complementary DNAs (cDNAs) of arginine vasotocin (AVT) and isotocin (IT) in a temperate wrasse (Halichoeres tenuispinis) and examined the effects of day/night and temperature on their expression in the diencephalon, because these neurohypophysial peptides are related to the sex behavior of wrasses. The full-length cDNAs of pro-AVT and pro-IT were 938 base pairs (154 amino acids) and 759 base pairs (156 amino acids) in length, respectively. Both pro-peptides contained a signal sequence followed by the respective hormones and neurophysin connected by a Gly–Lys–Arg bridge. Reverse-transcription polymerase chain reaction (RT-PCR) revealed that pro-AVT mRNA expression was specifically observed in the diencephalon, whereas pro-IT mRNA expression was seen in the whole brain. Quantitative RT-PCR revealed that the mRNA abundance of pro-AVT and pro-IT was higher at midday (zeitgeber time 6; ZT6) than at midnight (ZT18) under 12 h light and 12 h darkness (LD 12:12) conditions, but not under constant light. Intraperitoneal injection of melatonin decreased the mRNA abundance of pro-AVT, but not of pro-IT. When fish were reared under LD 12:12 conditions at 25, 20, and 15 °C, day high and night low mRNA expressions of pro-AVT and pro-IT were maintained. A field survey revealed seasonal variation in the number of swimming fish at observatory sites; many fish emerged from the sandy bottom in summer, but not in winter, suggesting a hibernation-like state under the sandy bottom under low temperature conditions. We conclude that the day–night fluctuation of pro-AVT and pro-IT mRNA abundance in the brain is not affected by temperature and repeated under the sandy bottom in winter.


Arginine vasotocin Circadian Hibernation Isotocin Melatonin qPCR Temperature 



This study was supported in part by a Grant-in-Aid for Scientific Research (B) (KAKENHI, grant number 16H05796) from the Japan Society for the Promotion of Science (JSPS) to AT and Heiwa Nakajima Foundation to AT, and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2012R1A6A3A04041089) to SPH.


  1. Bastian J, Schniederjan S, Nguyenkim J (2001) Arginine vasotocin modulates a sexually dimorphic communication behavior in the weakly electric fish Apteronotus leptorhynchus. J Exp Biol 204(Pt 11):1909–1923PubMedGoogle Scholar
  2. Carneiro LA, Oliveira R, Canário AVM, Grober MS (2003) The effect of arginine vasotocin on courtship behaviour in a blenniid fish with alternative reproductive tactics. Fish Physiol Biochem 28(1–4):241–243. CrossRefGoogle Scholar
  3. Clements JA, Funder JW (1986) Arginine vasopressin (AVP) and AVP-like immunoreactivity in peripheral tissues. Endocr Rev 7(4):449–460. CrossRefPubMedGoogle Scholar
  4. Gilchriest BJ, Tipping DR, Levy A, Baker BI (1998) Diurnal changes in the expression of genes encoding for arginine vasotocin and pituitary pro-opiomelanocortin in the rainbow trout (Oncorhynchus mykiss): correlation with changes in plasma hormones. J Neuroendocrinol 10(12):937–943. CrossRefPubMedGoogle Scholar
  5. Godwin J, Thompson R (2012) Nonapeptides and social behavior in fishes. Horm Behav 61(3):230–238. CrossRefPubMedGoogle Scholar
  6. Godwin J, Sawby R, Warner RR et al (2000) Hypothalamic arginine vasotocin mRNA abundance variation across sexes and with sex change in a coral reef fish. Brain Behav Evol 55(2):77–84. CrossRefPubMedGoogle Scholar
  7. Goodson JL, Bass AH (2001) Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Rev 35(3):246–265. CrossRefPubMedGoogle Scholar
  8. Goodson JL, Evans AK, Bass AH (2003) Putative isotocin distributions in sonic fish: relation to vasotocin and vocal-acoustic circuitry. J Comp Neurol 462(1):1–14. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Gozdowska M, Kleszczynska A, Sokołowska E, Kulczykowska E (2006) Arginine vasotocin (AVT) and isotocin (IT) in fish brain: diurnal and seasonal variations. Comp Biochem Physiol B 143(3):330–334. CrossRefPubMedGoogle Scholar
  10. Heierhorst J, Morley SD, Figueroa J, Krentler C, Lederis K, Richter D (1989) Vasotocin and isotocin precursors from the white sucker, Catostomus commersoni: cloning and sequence analysis of the cDNAs. Proc Natl Acad Sci USA 86(14):5242–5246. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Hiraoka S, Ando H, Ban M et al (1997) Changes in expression of neurohypophysial hormone genes during spawning migration in chum salmon, Oncorhynchus keta. J Mol Endocrinol 18(1):49–55. CrossRefPubMedGoogle Scholar
  12. Hur S-P, Takeuchi Y, Esaka Y et al (2011) Diurnal expression patterns of neurohypophysial hormone genes in the brain of the threespot wrasse Halichoeres trimaculatus. Comp Biochem Physiol A 158(4):490–497. CrossRefGoogle Scholar
  13. Hur S-P, Takeuchi Y, Itoh H et al (2012) Fish sleeping under sandy bottom: interplay of melatonin and clock genes. Gen Comp Endocrinol 177(1):37–45. CrossRefPubMedGoogle Scholar
  14. Hyodo S, Urano A (1991) Changes in expression of provasotocin and proisotocin genes during adaptation to hyper- and hypo-osmotic environments in rainbow trout. J Comp Physiol B 161(6):549–556. CrossRefPubMedGoogle Scholar
  15. Kulczykowska E (1999) Diel changes in plasma arginine vasotocin, isotocin, and melatonin in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 21(2):141–146. CrossRefGoogle Scholar
  16. Kulczykowska E (2001) A review of the multifunctional hormone melatonin and a new hypothesis involving osmoregulation. Rev Fish Biol Fish 11:321–330CrossRefGoogle Scholar
  17. Kulczykowska E, Stolarski J (1996) Diurnal changes in plasma arginine vasotocin and isotocin in rainbow trout adapted to fresh water and brackish Baltic water. Gen Comp Endocrinol 104(2):197–202. CrossRefPubMedGoogle Scholar
  18. Kulczykowska E, Warne JM, Balment RJ (2001) Day-night variations in plasma melatonin and arginine vasotocin concentrations in chronically cannulated flounder (Platichthys flesus). Comp Biochem Physiol A 130(4):827–834. CrossRefGoogle Scholar
  19. Lema S, Nevitt G (2004) Variation in vasotocin immunoreactivity in the brain of recently isolated populations of a death valley pupfish, Cyprinodon nevadensis. Gen Comp Endocrinol 135(3):300–309. CrossRefPubMedGoogle Scholar
  20. Motohashi E, Hamabata T, Ando H (2008) Structure of neurohypophysial hormone genes and changes in the levels of expression during spawning season in grass puffer (Takifugu niphobles). Gen Comp Endocrinol 155(2):456–463. CrossRefPubMedGoogle Scholar
  21. Nishi G (1989) Locomotor activity rhythm in two wrasses, Halichoeres tenuispinnis and Pteragogus flagellifera, under various light conditions. Jpn J Ichthyol 36(3):350–356. CrossRefGoogle Scholar
  22. Nishi G (1990) Locomotor activity rhythm in four wrasse species under varying light conditions. Jpn J Ichthyol 37:170–181. CrossRefGoogle Scholar
  23. Nishi G (1991) The relationship between locomotor activity rhythm and burying behavior in the wrasse, Suezichthys gracilis. Jpn J Ichthyol 37:402–409. CrossRefGoogle Scholar
  24. O’Connell LA, Matthews BJ, Hofmann HA (2012) Isotocin regulates paternal care in a monogamous cichlid fish. Horm Behav 61(5):725–733. CrossRefPubMedGoogle Scholar
  25. Ota Y, Ando H, Ueda H, Urano A (1999) Seasonal changes in expression of neurohypophysial hormone genes in the preoptic nucleus of immature female masu salmon. Gen Comp Endocrinol 116(1):31–39. CrossRefPubMedGoogle Scholar
  26. Randall JE (1999) Halichoeres bleekeri (steindachner & döderlein), a valid Japanese species of labrid fish, distinct from H. tenuispinis (Günther) from China. Ichthyol Res 46(3):225–231. CrossRefGoogle Scholar
  27. Rodríguez-Illamola A, López Patiño MA, Soengas JL, Ceinos RM, Míguez JM (2011) Diurnal rhythms in hypothalamic/pituitary AVT synthesis and secretion in rainbow trout: evidence for a circadian regulation. Gen Comp Endocrinol 170(3):541–549. CrossRefPubMedGoogle Scholar
  28. Ruoff P, Rensing L (2004) Temperature effects on circadian clocks. J Therm Biol 29(7-8):445–456. CrossRefGoogle Scholar
  29. Saito D, Shi Q, Ando H, Urano A (2004) Attenuation of diurnal rhythms in plasma levels of melatonin and cortisol, and hypothalamic contents of vasotocin and isotocin mRNAs in pre-spawning chum salmon. Gen Comp Endocrinol 137(1):62–68. CrossRefPubMedGoogle Scholar
  30. Salek SJ, Sullivan CV, Godwin J (2002) Arginine vasotocin effects on courtship behavior in male white perch (Morone americana). Behav Brain Res 133(2):177–183. CrossRefPubMedGoogle Scholar
  31. Santangelo N, Bass AH (2010) Individual behavioral and neuronal phenotypes for arginine vasotocin mediated courtship and aggression in a territorial teleost. Brain Behav Evol 75(4):282–291. CrossRefPubMedGoogle Scholar
  32. Semsar K, Kandel FL, Godwin J (2001) Manipulations of the AVT system shift social status and related courtship and aggressive behavior in the bluehead wrasse. Horm Behav 40(1):21–31. CrossRefPubMedGoogle Scholar
  33. Thompson RR, Walton JC (2004) Peptide effects on social behavior: effects of vasotocin and isotocin on social approach behavior in male goldfish (Carassius auratus). Behav Neurosci 118(3):620–626. CrossRefPubMedGoogle Scholar
  34. Urano A, Ando H (2011) Diversity of the hypothalamo-neurohypophysial system and its hormonal genes. Gen Comp Endocrinol 170(1):41–56. CrossRefPubMedGoogle Scholar
  35. Van den Dungen HM, Buijs RM, Pool CW, Terlou M (1982) The distribution of vasotocin and isotocin in the brain of the rainbow trout. J Comp Neurol 212(2):146–157. CrossRefPubMedGoogle Scholar
  36. Warne JM, Hyodo S, Harding K, Balment RJ (2000) Cloning of pro-vasotocin and pro-isotocin cDNAs from the flounder Platichthys flesus; levels of hypothalamic mRNA following acute osmotic challenge. Gen Comp Endocrinol 119(1):77–84. CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Chemistry, Biology and Marine Science, Faculty of ScienceUniversity of the RyukyusOkinawaJapan
  2. 2.Jeju International Marine Science Research & Education CenterKorea Institute of Ocean Science & TechnologyJeju Special Self-Governing ProvinceSouth Korea
  3. 3.Developmental Neurobiology Unit, Okinawa Institute of Science and Technology Graduate UniversityOnna-sonJapan
  4. 4.Marine Science InstituteJeju National UniversityJeju Special Self-Governing ProvinceSouth Korea

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