Diurnal rhythms of behavior and brain mRNA expression for arginine vasotocin, isotocin, and their receptors in wild amargosa pupfish (Cyprinodon nevadensis amargosae)

Marine and Freshwater Behaviour and Physiology

Volumn 43, Issue 4, 2010, Pages 257-281

  Lema, Sean C ^a   Wagstaff, Lauren J ^a   Gardner, Nina M ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

AVT; Behavior; Cyprinodon nevadensis amargosae; Diel variation; Fish; Isotocin; Receptor; Vasotocin

Indexed keywords

ABUNDANCE; BEHAVIORAL ECOLOGY; COURTSHIP; DIEL MIGRATION; DIURNAL VARIATION; ENVIRONMENTAL CONDITIONS; FISH; RNA; SPAWNING;

CYPRINODON NEVADENSIS; CYPRINODON NEVADENSIS AMARGOSAE;

EID: 77955867867     PISSN: 10236244     EISSN: 10290362     Source Type: Journal    
DOI: 10.1080/10236244.2010.498632     Document Type: Article

References (85)

1. Adams CF, Foy RJ, Kelley JJ, Coyle KO. 2009. Seasonal changes in the diel vertical migration of walleye pollock (Theragra chalcogramma) in the northern Gulf of Alaska. Environ Biol Fish. 86(2):297-305.
2. Baker BI, Bird DJ, Buckingham JC. 1996. In the trout, CRH and AVT synergize to stimulate ACTH release. Reg Peptides. 67:207-210.
3. Balment RJ, Lu W, Weybourne E, Warne JM. 2006. Arginine vasotocin a key hormone in fish physiology and behaviour: a review with insights from mammalian models. Gen Comp Endocrinol. 147:9-16.
4. Barlow GW. 1958. Daily movements of desert pupfish, Cyprinodon macularius, in shore pools of the Salton sea, California. Ecology. 39(4):580-587.
5. Barlow GW. 1961. Social behavior of the desert pupfish, Cyprinodon macularius, in the field and in the aquarium. Amer Mid Nat. 65(2):339-359.
6. Blanco-Vives B, Sanchez-Vazquez FJ. 2009. Synchronisation to light and feeding time of circadian rhythms of spawning and locomotor activity in zebrafish. Physiol Behav. 98(3):268-275.
7. Brown JH, Feldmeth R. 1971. Evolution in constant and fluctuating environments: thermal tolerances of desert pupfish (Cyprinodon). Evolution. 25(2):390-398.
8. Caldwell HK, Albers EH. 2004a. Photoperiodic regulation of vasopressin receptor binding in female Syrian hamsters. Brain Res. 1002:136-141.
9. Caldwell HK, Albers EH. 2004b. Effect of photoperiod on vasopressin-induced aggression in Syrian hamsters. Horm Behav. 46:444-449.
10. Caldwell HK, Lee H-J, Macbeth AH, Young III WS. 2008a. Vasopressin: behavioral roles of an "original" neuropeptide. Prog Neurobiol. 84:1-24.
11. Caldwell HK, Smith DA, Albers EH. 2008b. Photoperiodic mechanism controlling scent marking: interactions of vasopressin and gonadal steroids. Eur J Neurosci. 27:1189-1196.
12. Delville Y, Mansour KM, Ferris CF. 1996. Testosterone facilitates aggression by modulating vasopressin receptors in the hypothalamus. Physiol Behav. 60:25-29.
13. Dewan AK, Maruska KP, Tricas TC. 2008. Arginine vasotocin neuronal populations among congeneric territorial and shoaling reef butterflyfishes: species, sex and reproductive season comparisons. J Neuroendocrinol. 20:1382-1394.
14. Duarte G, Segura-Noguera MM, Martin del Rio MP, Mancera JM. 2001. The hypothalamohypophyseal system of the white sea bream Diplodus sargus: immunocytochemical identification of arginine vasotocin, isotocin, melanin-concentrating hormone and corticotrophin-releasing factor. Histochem J. 33:569-578.
15. Duncan MJ, Cheng X, Heller KS. 1995. Photoperiodic exposure and time of day modulate the expression of arginine vasopressin mRNA and vasoactive intestinal peptide mRNA in the suprachiasmatic nuclei of Siberian hamsters. Brain Res Mol Brain Res. 32:181-186.
16. Falcón J, Besseau L, Sauzet S, Boeuf G. 2007. Melatonin effects on the hypothalamo-pituitary axis in fish. Trends Endocrinol Metabol. 18(2):81-88.
17. Falcón J, Migaud H, Muñoz-Cueto JA, Carrillo M. 2010. Current knowledge on the melatonin system in teleost fish. Gen Comp Endocinol. 165:469-482.
18. Feldmeth CR. 1981. The evolution of thermal tolerance in desert pupfish (genus: Cyprinodon). In: Naiman RJ, Soltz DL, editors. Fishes in North American deserts. New York: John Wiley & Sons, Chapter 11. p. 357-384.
19. Ferris CF, Melloni RH, Koppel G, Perry KW, Fuller RW, Delville Y. 1997. Vasopressin/ serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. J Neurosci. 17:4331-4340.
20. Ferris CF, Potegal M. 1988. Vasopressin receptor blockage in the anterior hypothalamus suppresses aggression in hamsters. Physiol Behav. 44:235-239.
21. Foran CM, Bass AH. 1998. Preoptic AVT immunoreactive neurons of a teleost fish with alternative reproductive tactics. Gen Comp Endocrinol. 111:271-282.
22. Fraser NHC, Metcale NB, Thorpe JE. 1993. Temperature-dependent switch between diurnal and nocturnal foraging in salmon. Proc Roy Soc Lond B. 252(1334):135-139.
23. Gilchriest BJ, Tipping DR, Hake L, Levy A, Baker BI. 2000. The effects of acute and chronic stresses on vasotocin gene transcripts in the brain of the rainbow trout (Oncorhynchus mykiss). J Neuroendocrinol. 12:795-801.
24. 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. 10:937-943.
25. Godwin J, Sawby R, Warner RR, Crews D, Grober MS. 2000. Hypothalamic arginine vasotocin mRNA abundance variation across sexes and with sex change in a coral reef fish. Brain Behav Evol. 55:77-84.
26. Goodson JL, Bass AH. 2000. Forebrain peptides modulate sexually polymorphic vocal circuitry. Nature. 403:769-772.
27. Goodson JL, Bass AH. 2001. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Rev. 35:246-265.
28. Goossens N, Dierickx K, Vandesande F. 1977. Immunocytochemical localization of vasotocin and isotocin in the preopticohypophysial neurosecretory system of teleosts. Gen Comp Endocrinol. 32:371-375.
29. Gozdowska M, Kleszczyń ska A, Sokolowska E, Kulczykowska E. 2006. Arginine vasotocin (AVT) and isotocin (IT) in fish brain: diurnal and seasonal variations. Comp Biochem Physiol B. 143:330-334.
30. Greenwood AK, Wark AR, Fernald RD, Hofmann HA. 2008. Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish. Proc Roy Soc B. 275(1649):2393-2402.
31. Grober MS, George AA, Watkins KK, Carneiro LA, Oliveira RF. 2002. Forebrain AVT and courtship in a fish with male alternative reproductive tactics. Brain Res Bull. 57:423-425.
32. Hansen EA, Closs GP. 2005. Diel activity and home range size in relation to food supply in a drift-feeding stream fish. Behav Ecol. 16(3):640-648.
33. Helfman GS. 1993. Fish behaviour by day, night and twilight. In: Pitcher TJ, editor. Behaviour of teleost fishes. London: Chapman and Hall. p. 479-512.
34. Hibino M, Ohta T, Isoda T, Nakayama K, Tanaka M. 2006. Diel and tidal changes in the distribution and feeding habits of Japanese temperate bass Lateokabrax japonicus juveniles in the surf zone of Ariake Bay. Ichthyol Res. 53(2):129-136.
35. Hontela A, Lederis K. 1985. Diel variations in arginine vasotocin content of goldfish brain and pituitary: effects of photoperiod and pinealectomy. Gen Comp Endocrinol. 57:397-404.
36. Itzkowitz M. 1974. The effects of other fish on the reproductive behavior of the male Cyprinodon variegatus (Pisces: Cyprinodontidae). Behaviour. 48:1-21.
37. James CJ. 1969. Aspects of the ecology of the Devil's Hole pupfish, Cyprinodon diabolis [MS thesis]. [Las Vegas (NV)]: University of Nevada.
38. Kadri S, Metcalfe NB, Huntingford FA, Thorpe JE. 1997. Daily feeding rhythms in Atlantic salmon II: size-related variation in feeding patterns of post-smolts under constant environmental conditions. J Fish Biol. 50:273-279.
39. Kalamatianos T, Kallo I, Coen CW. 2004. Ageing and the diurnal expression of the mRNAs for vasopressin and for the V1a and V1b vasopressin receptors in the suprachiasmatic nucleus of male rats. J Neuroendocrinol. 16(6):493-501.
40. Kodric-Brown A. 1978. Establishment and defense of breeding territories in a pupfish (Cyprinodontidae: Cyprinodon). Anim Behav. 26:818-834.
41. Kodric-Brown A. 1981. Variable breeding systems in pupfish (genus: Cyprinodon): adaptations to changing environments. In: Naiman RJ, Soltz DL, editors. Fishes in North American deserts. New York: John Wiley & Sons, Chapter 7. p. 205-235.
42. Konno N, Hyodo S, Yamaguchi Y, Kaiya H, Miyazato M, Matsuda K, Uchiyama M. 2009. African lungfish, Protopterus annectens, possess an arginine vasotocin receptor homologous to the tetrapod V2-type receptor. J Exp Biol. 212:2183-2193.
43. Konno N, Hyodo S, Yamaguchi Y, Matsuda K, Uchiyama M. 2010. Vasotocin/V2-type receptor/aquaporin axis exists in African lungfish kidney but is functional only in terrestrial condition. Endocrinol. 151:1089-1096.
44. Kulczykowska E. 1999. Diel changes in plasma arginine vasotocin, isotocin, and melatonin in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem. 21:141-146.
45. Kulczykowska E, Stolarski J. 1996. Diurnal changes in plasma vasotocin and isotocin in rainbow trout adapted to fresh water and brackish Baltic water. Gen Comp Endocrinol. 104:197-202.
46. 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. 130:827-834.
47. Larson ET, O'Malley DM, Melloni Jr RH. 2006. Aggression and vasotocin are associated with dominant-subordinate relationships in zebrafish. Behav Brain Res. 167:94-102.
48. Leiser JK. 2003. When are neighbors 'dear enemies' and when are they not? The responses of territorial male variegated pupfish, Cyprinodon variegatus, to neighbors, strangers and heterospecifics. Anim Behav. 65:453-462.
49. Leiser JK, Itzkowitz M. 2003. The breeding system of an endangered pupfish (Cyprindon elegans). Wester N Amer Nat. 63(1):118-121.
50. Lema SC. 2006. Population divergence in plasticity of the AVT system and its association with aggressive behaviors in a Death Valley pupfish. Horm Behav. 50:183-193.
51. Lema SC. 2008. The phenotypic plasticity of Death Valley's pupfish. Amer Sci. 96:28-36.
52. Lema SC. 2010. Identification of multiple vasotocin receptor cDNAs in teleost fish: sequences, phylogenetic analysis, sites of expression, and regulation in the hypothalamus and gill in response to acute hyperosmotic challenge. Mol Cell Endocrinol. 321:215-230.
53. Lema SC, Nevitt GA. 2004a. Exogenous vasotocin alters aggression during agonistic exchanges in male Amargosa River pupfish (Cyprinodon nevadensis amargosae). Horm Behav. 46:628-637.
54. Lema SC, Nevitt GA. 2004b. Variation in vasotocin immunoreactivity in the brain of recently isolated populations of a Death Valley pupfish, Cyprinodon nevadensis. Gen Comp Endocrinol. 135:300-309.
55. Li J-D, Burton KJ, Zhang C, Hu S-B, Zhou Q-Y. 2009. Vasopressin receptor V1a regulates circadian rhythms of locomotor activity and expression of clock-controlled genes in the suprachiasmatic nuclei. Am J Physiol Regul Comp Physiol. 296:R824-R830.
56. Liu RK. 1969. The comparative behavior of allopatric species (Teleostei - Cyprinodontidae: Cyprinodon) [PhD thesis]. [Los Angeles (CA)]: University of California.
57. Mahoney MM, Ramanathan C, Hagenauer MH, Thompson RC, Smale L, Lee T. 2009. Daily rhythms and sex differences in vasoactive intestinal polypeptide, VIPR2 receptor and arginine vasopressin mRNA in the suprachiasmatic nucleus of a diurnal rodent, Arvicanthis niloticus. Eur J Neurosci. 30:1537-1543.
58. Mihai R, Coculescu M, Wakerley JB, Ingram CD. 1994. The effects of [Arg8]vasopressin and [Arg8]vasotocin on the firing rate of suprachiasmaic neurons in vitro. Neurosci. 62(3):783-792.
59. Miranda JA, Oliveira RF, Carneiro LA, Santos RS, Grober MS. 2003. Neurochemical correlates of male polymorphism and alternative reproductive tactics in the Azorean rock-pool blenny, Parablennius parvicornis. Gen Comp Endocrinol. 132:183-189.
60. Patchev VK, Almeida OF. 1995. Corticosteroid regulation of gene expression and binding characteristics of vasopressin receptors in the rat brain. Eur J Neurosci. 7:1579-1583.
61. Pister EP. 1981. The conservation of desert fishes. In: Naiman RJ, Soltz DL, editors. Fishes in North American deserts. New York: John Wiley & Sons, Chapter 13. p. 411-445.
62. Pfaff MW. 2001. A new mathematical model for relative quantification in realtime RT-PCR. Nuc Acids Res. 29:2002-2007.
63. Raney EC, Backus RH, Crawford RW, Robins CR. 1953. Reproductive behavior in Cyprinodon variegatus Lacépède, in Florida. Zoologica. 38:97-104.
64. Rasmussen R. 2000. Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K, editors. Rapid cycle real-time PCR, methods and applications. Heidelberg: Springer Press. p. 21-34.
65. Reebs SG. 2002. Plasticity of diel and circadian activity rhythms in fishes. Rev Fish Biol Fish. 12(4):349-371.
66. 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. 137:62-68.
67. Salek SJ, Sullivan CV, Godwin J. 2002. Arginine vasotocin effects on courtship behavior in male white perch (Morone americana). Behav Brain Res. 133:177-183.
68. Santangelo N, Bass AH. 2006. New insights into neuropeptide modulation of aggression: field studies of arginine vasotocin in a territorial tropical damselfish. Proc R Soc B. 273:3085-3092.
69. Schoenherr AA. 1981. The role of competition in the replacement of native fishes by introduced species. In: Hocutt CH, Wiley EO, editors. Fishes in North American deserts. New York: John Wiley & Sons, Chapter 6. p. 173-203.
70. Scoppettone GG, Rissler PH, Gourley C, Martinez C. 2005. Habitat restoration as means of controlling non-native fish in a Mojave Desert oasis. Restoration Ecol. 13(2):247-256.
71. Semsar K, Kandel FLM, Godwin J. 2001. Manipulations of the AVT system shift social status and related courtship and aggressive behavior in the bluehead wrasse. Horm Behav. 40:21-31.
72. Smith GW, Glass CW, Johnstone ADF, Mojsiewicz WR. 1993. Diurnal patterns in the spatial relationships between saithe, Pollachius virens, schooling in the wild. J Fish Biol. 43(suppl. A):315-325.
73. Sogard SM, Olla BL. 1996. Diel patterns of behavior in juvenile walleye Pollock, Theragra chalcogramma. Environ Biol Fish. 47(4):379-386.
74. Soltz DL. 1974. Variation in life history and social organization of some populations of Nevada pupfish, Cyprinodon nevadensis [PhD thesis]. [Los Angeles (CA)]: University of California.
75. Soltz DL, Naiman RJ. 1978. The natural history of native fishes in the Death Valley system. Nat Hist Mus Los Angeles County Sci Ser. 30:1-76.
76. 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.
77. Thurow RF. 1997. Habitat utilization and diel behavior of juvenile bull trout (Salvelinus confluentus) at the onset of winter. Ecol Fresh Fish. 6:1-7.
78. Tominaga K, Shinohara K, Otori Y, Fukuhara C, Inouye ST. 1992. Circadian rhythms of vasopressin content in the suprachiasmatic nucleus of the rat. NeuroReport. 3:809-812.
79. Uhl GR, Reppert SM. 1986. Suprachiasmatic nucleus vasopressin messenger RNA: circadian variation in normal and Brattleboro rats. Science. 232:390-393.
80. 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. 212:146-157.
81. Walton JC, Waxman B, Hoffbuhr K, Kennedy M, Beth E, Scangos J, Thompson RR. 2010. Behavioral effects of hindbrain vasotocin in goldfish are seasonally variable but not sexually dimorphic. Neuropharmacology. 58(1):126-134.
82. Warne J. 2002. The role of arginine vasotocin in teleost fish osmoregulation. In: Hazon N, Flick G, editors. Osmoregulation and drinking in vertebrates. Oxford (UK): BIOS Scientific Publishers, Ltd, Chapter 6. p. 83-95.
83. Watters JJ, Wilkinson CW, Dorsa DM. 1996. Glucocorticoid regulation of vasopressin V1a receptors in rat forebrain. Mol Brain Res. 38:276-284.
84. Yambe Y, Arima H, Kakiya S, Murase T, Oiso Y. 2002. Diurnal changes in arginine vasopressin gene transcription in the rat suprachiasmatic nucleus. Mol Brain Res. 104:132-136.
85. Young LJ, Wang Z, Cooper TT, Albers HE. 2000. Vasopressin receptor (V1a) binding, mRNA expression and transcriptional regulation by androgen in the Syrian hamster brain. J Neuroendocrinol. 12:1179-1185.