Fish and chips: Functional genomics of social plasticity in an African cichlid fish

Journal of Experimental Biology

Volumn 211, Issue 18, 2008, Pages 3041-3056

  Renn, Susan C P ^a,b   Aubin Horth, Nadia ^a,c   Hofmann, Hans A ^a,d  

^a HARVARD UNIVERSITY   (United States)

^b REED COLLEGE   (United States)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Behavior; Cichlid; Microarray; Plasticity; Social behavior

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BAYES THEOREM; CICHLID; CLUSTER ANALYSIS; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; GENETICS; GENOMICS; MALE; PHENOTYPE; PHYSIOLOGY; REPRODUCTION; SOCIAL BEHAVIOR; SOCIAL DOMINANCE;

ANIMALS; BAYES THEOREM; BEHAVIOR, ANIMAL; CICHLIDS; CLUSTER ANALYSIS; DOMINANCE-SUBORDINATION; FEMALE; GENE EXPRESSION PROFILING; GENETIC VARIATION; GENOMICS; HIERARCHY, SOCIAL; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; REPRODUCTION; SOCIAL BEHAVIOR;

AFRICAN CICHLIDS; ASTATOTILAPIA BURTONI; CICHLIDAE;

EID: 53549130568     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.018242     Document Type: Article

References (112)

1. Amano, M., Hyodo, S., Kitamura, S., Ikuta, K., Suzuki, Y., Urano, A. and Aida, K. (1995). Short photoperiod accelerates preoptic and ventral telencephalic salmon GnRH synthesis and precocious maturation in underyearling male masu salmon. Gen. Comp. Endocrinol. 99, 22-27.
2. Arnold, A. P. (1992). Hormonally-induced alterations in synaptic organization in the adult nervous-system. Exp. Gerontol. 27, 99-110.
3. Au, T. M., Anna, K. G. and Fernald, R. D. (2006). Differential social regulation of two pituitary gonadotropin-releasing hormone receptors. Behav. Brain Res. 170, 342-346.
4. Aubin-Horth, N., Landry, C. R., Letcher, B. H. and Hofmann, H. A. (2005). Alternative life histories shape brain gene expression profiles in males of the same population. Proc. R. Soc. Lond. B 272, 1655-1662.
5. Aubin-Horth, N., Desjardins, J. K., Martei, Y. M., Balshine, S. and Hofmann, H. A. (2007). Masculinized dominant females in a cooperatively breeding species. Mol. Ecol. 16, 1349-1358.
6. Black, M. P., Balthazart, J., Baillien, M. and Grober, M. S. (2005). Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex-changing fish, Lythrypnus dalli. Proc. Biol. Sci. 272, 2435-2440.
7. Brem, R. B., Yvert, G., Clinton, R. and Kruglyak, L. (2002). Genetic dissection of transcriptional regulation in budding yeast. Science 296, 752-755.
8. Buckley, B. A., Gracey, A. Y. and Somero, G. N. (2006). The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. J. Exp. Biol. 209, 2660-2677.
9. Burmeister, S. S., Jarvis. E. D. and Fernald, R. D. (2005). Rapid behavioral and genomic responses to social opportunity. PLoS Biol. 3, 1996-2004.
10. Burmeister, S. S., Kailasanath, V. and Fernald, R. D. (2007). Social dominance regulates androgen and estrogen receptor gene expression. Horm. Behav. 51, 164-170.
11. Carneiro, L. A., Oliveira, R. F., Canario, A. V. M. and Grober, M. S. (2003). The effect of arginine vasotocin on courtship behaviour in a blenniid fish with alternative reproductive tactics. Fish Physiol. Biochem. 28, 241-243.
12. Churchill, G. A. (2002). Fundamentals of experimental design for cDNA microarrays. Nat. Genet. 32, 490-495.
13. Chu, Z. G. and Moenter, S. M. (2005). Endogenous activation of metabotropic glutamate receptors modulates GABAergic transmission to gonadotropin-releasing hormone neurons and alters their firing rate: a possible local feedback circuit. J. Neurosci. 25, 5740-5749.
14. Clark, T. A. and Townsend, J. P. (2007). Quantifying variation in gene expression. Mol. Ecol. 16, 2613-2616.
15. Clarkson, J. and Herbison, A. E. (2006). Development of GABA and glutamate signaling at the GnRH neuron in relation to puberty. Mol. Cell. Endocrinol. 254, 32-38.
16. Cummings, M. E., Larkins-Ford, J., Reilly, C. R. L., Wong, R. Y., Ramsey, M. and Hofmann, H. A. (2008). Sexual and social stimuli elicit rapid and contrasting genomic responses. Proc. Biol. Sci. 275, 393-402.
17. Davis, M. R. and Fernald, R. D. (1990). Social control of neuronal soma size. J. Neurobiol. 21, 1180-1188.
18. Dawson, A., King, V. M., Bentley, G. E. and Ball, G. F. (2001). Photoperiodic control of seasonality in birds. J. Biol. Rhythms 16, 365-380.
19. Devoogd, T. and Nottebohm, F. (1981). Gonadal-hormones induce dendritic growth in the adult avian brain. Science 214, 202-204.
20. Fernald, R. D. (1977). Quantitative behavioural observations of Haplochromis burtoni under semi-natural conditions. Anim. Behav. 25, 643-653.
21. Fernald, R. D. (2002). Social regulation of the brain: sex, size and status. In Genetics and Biology of Sex Determination no. 244 (ed. Novartis Foundation), pp. 169-186. Chichester: John Wiley and Sons.
22. Fernald, R. D. (2004). Social influences on the brain. Horm. Behav. 46, 129-130.
23. Fernald, R. D. and Hirata, N. R. (1977a). Field study of Haplochromis burtoni: quantitative behavioral observations. Anim. Behav. 25, 964-975.
24. Fernald, R. D. and Hirata, N. R. (1977b). Field study of Haplochromis burtoni: habitats and co-habitants. Environ. Biol. Fishes 2, 299-308.
25. Fodor, J. A. (1983). The Modularity of Mind. Cambridge, MA: The MIT Press.
26. Forsyth, I. A. and Wallis, M. (2002). Growth hormone and prolactin-molecular and functional evolution. J. Mammary Gland Biol. Neoplasia 7, 291-312.
27. Fox, H. E., White, S. A., Kao, M. H. F. and Fernald, R. D. (1997). Stress and dominance in a social fish. J. Neurosci. 17, 6463-6469.
28. Francis, R. C., Soma, K. and Fernald, R. D. (1993). Social regulation of the brain pituitary-gonadal axis. Proc. Natl. Acad. Sci. USA 90, 7794-7798.
29. Fukamachi, S. and Sugimoto, M. (2004). Identification of the gene for morphological body-color change: Somatolactin. Zool. Sci. 21, 1224.
30. Gabriel, S. M., Koenig, J. I. and Washton, D. L. (1993). Estrogen stimulation of galanin gene-expression and galanin-like immunoreactivity in the rat and its blockade by the estrogen antagonist keoxifene. Regul. Pept. 45, 407-419.
31. Ge, Y. C., Dudoit, S. and Speed, T. P. (2003). Resampling-based multiple testing for microarray data analysis. Test 12, 1-77.
32. Gerst, J. E. (1999). SNAREs and SNARE regulators in membrane fusion and exocytosis. Cell. Mol. Life Sci. 55, 707-734.
33. Goodson, J. L. (1998). Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav. 34, 67-77.
34. Goodson, J. L. and Adkins-Regan, E. (1999). Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata). J. Neuroendocrinol. 11, 19-25.
35. Goodson, J. L. and Bass, A. H. (2001). Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res. Rev. 35, 246-265.
36. Greenwood, A. K. and Fernald, R. D. (2004). Social regulation of the electrical properties of gonadotropin-releasing hormone neurons in a Cichlid fish (Astatotilapia burtoni). Biol. Reprod. 71, 909-918.
37. Greenwood, A. K., Wark, A. R., Fernald, R. D. and Hofmann, H. A. (2008). Arginine vasotocin mediates both dominant and subordinate behavior via two distinct preoptic pathways. Proc. Biol. Sci. doi:10.10981/rspb.2008. 0622
38. Grober, M. S., George, A. A., Watkins, K. K., Carneiro, L. A. and Oliveira, R. F. (2002). Forebrain AVT and courtship in a fish with male alternative reproductive tactics. Brain Res. Bull. 57, 423-425.
39. Grozinger, C. M. and Robinson, G. E. (2002). Microarray analysis of pheromone-mediated gene expression in the honey bee brain. Integr. Comp. Bid. 42, 1237-1237.
40. Hallgren, S. L. E., Linderoth, M. and Olsen, K. H. (2006). Inhibition of cytochrome p450 brain aromatase reduces two male specific sexual behaviours in the male Endler guppy (Poecilia reticulata). Gen. Comp. Endocrinol. 147, 323-328.
41. Hartwell, L. H., Hopfield, J. J., Leibler, S. and Murray, A. W. (1999). From molecular to modular cell biology. Nature 402, C47-C52.
42. Helle, K. B. (2004). The granin family of uniquely acidic proteins of the diffuse neuroendocrine system: comparative and functional aspects. Biol. Rev. 79, 769-794.
43. Hofmann, H. A. (2003). Functional Genomics of Neural and Behavioral Plasticity. J. Neurobiol. 54, 272-282.
44. Hofmann, H. A. (2006). GnRH signaling in behavioral plasticity. Curr. Opin. Neurobiol. 16, 343-350.
45. Hofmann, H. A. and Fernald, R. D. (2000). Social status controls somatostatin neuron size and growth. J. Neurosci. 20, 4740-4744.
46. Hofmann, H. A., Benson, M. E. and Fernald, R. D. (1999a). Social status regulates growth rate: Consequences for life-history strategies. Proc. Natl. Acad. Sci. USA 96, 14171-14176.
47. Hofmann, H. A., Le Bail, P. Y. and Fernald, R. D. (1999b). Social control of growth and growth hormone levels in an African cichlid fish. Abstr. - Soc. Neurosci. 29, 348.16.
48. Holmes, A., Yang, R. J. and Crawley, J. N. (2002). Evaluation of an anxiety-related phenotype in galanin overexpressing transgenic mice. J. Mol. Neurosci. 18, 151-165.
49. Jadhao, A. and Pinelli, C. (2001). Galanin-like immunoreactivity in the brain and pituitary of the 'four-eyed' fish, Anableps anableps. Cell Tissue Res. 306, 309-318.
50. Johnsson, M., Axelsson, M. and Holmgren, S. (2001). Large veins in the Atlantic cod (Gadus morhua) and the rainbow trout (Oncorhynchus mykiss) are innervated by neuropeptide-containing nerves. Anat. Embryol. 204, 109-115.
51. Kageyama, H., Takenoya, F., Kita, T., Hori, T., Guan, H. L. and Shioda, S. (2005). Galanin-like peptide in the brain: effects on feeding energy metabolism and reproduction. Regul. Pept. 126, 21-26.
52. Kocher, T. D. (2004). Adaptive evolution and explosive speciation: The cichlid fish model. Nat. Rev. Genet. 5, 288-298.
53. Legac, F., Blaise, O., Fostier, A., Lebail, P. Y., Loir, M., Mourot, B. and Well, C. (1993). Growth-Hormone (GH) and Reproduction - a review. Fish Physiol. Biochem. 11, 219-232.
54. Lim, M. M., Hammock, E. A. and Young, L. J. (2004). The role of vasopressin in the genetic and neural regulation of monogamy. J. Neuroendocrinol. 16, 325-332.
55. Liu, H. H., Payne, H. R., Wang, B. and Brady, S. T. (2006). Gender differences in response of hippocampus to chronic glucocorticoid stress: Role of glutamate receptors. J. Neurosci. Res. 83, 775-786.
56. Maan, M. E., Eshuis, B., Haesler, M. P., Schneider, M. V., Van Alphen, J. J. M. and Seehausen, O. (2008). Color polymorphism and predation in a Lake Victoria cichlid fish. Copeia. 2008 (3), 621-629.
57. Madani, R., Kosloz, S., Akhmedov, A., Cinelli, P., Kinter, J., Lipp, H. P., Sonderegger, P. and Wolfer, D. P. (2003). Impaired explorative behavior in neophobia in genetically modified mice lacking or overexpressing the extracellular serine protease inhibitor neuroserpin. Mol. Cell. Neurosci. 23, 473-494.
58. Maere, S., Heymans, K. and Kuiper, M. (2005). BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks. Bioinformatics 21, 3448-3449.
59. Marsh, K. E., Creutz, L. M., Hawkins, M. B. and Godwin, J. (2006). Aromatase immunoreactivity in the bluehead wrasse brain, Thalassoma bifasciatum: Immunolocalization and co-regionalization with arginine vasotocin and tyrosine hydroxylase. Brain Res. 1126, 91-101.
60. Martyniuk, C. J., Xiong, H. L., Crump, K., Chiu, S., Sardana, R., Nadler, A., Gerrie, E. R., Xia, X. H. and Trudeau, V. L. (2006). Gene expression profiling in the neuroendocrine brain of male goldfish (Carassius auratus) exposed to 17 alpha-ethinylestradiol. Physiol. Genomics 27, 328-336.
61. Miranda, E. and Lomas, D. A. (2006). Neuroserpin: a serpin to think about. Cell. Mol. Life Sci. 63, 709-722.
62. Mrowk, A. (1984). Brood care motivation and hunger in the mouth brooding cichlid Pseudochrenilabrus multicolor. Behav. Processes 9, 181-190.
63. Munz, H. (1999). GnRH-systems in the forebrain of cichlid fish. Eur. J. Morphol. 37, 100-102.
64. Nakamura, M. and Kobayashi, Y. (2005). Sex change in coral reef fish. Fish Physiol. Biochem. 31, 117-122.
65. Nelson, R. J. (2005). An Introduction to Behavioral Endocrinology. 3rd edn. Sunderland, MA: Sinauer Associates.
66. Olazabal, D. E. and Young, L. J. (2006). Oxytocin receptors in the nucleus accumbens facilitate 'spontaneous' maternal behavior in adult female prairie voles. Neuroscience 141, 559-568.
67. Oliveira, R. F., Hirschenhauser, K., Carneiro, L. A. and Canario, A. V. M. (2002). Social modulation of androgen levels in male teleost fish. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 132, 203-215.
68. Op de Beeck, H. P., Haushofer, J. and Kanwisher, N. G. (2008). Interpreting fMRI data: maps, modules and dimensions. Nat. Rev. Neurosci. 9, 123-135.
69. Parhar, I. S., Ogawa, S. and Sakuma, Y. (2005). Three GnRH receptor types in laser-captured single cells of the cichlid pituitary display cellular and functional heterogeneity. Proc. Natl. Acad. Sci. USA 102, 2204-2209.
70. Parikh, V. N., Clement, T. S. and Fernald, R. D. (2006). Androgen level and male social status in the African cichlid, Astatotilapia burtoni. Behav. Brain Res. 166, 291-295.
71. Pollen, A. A., Dobberfuhl, A. P., Scace, J., Igulu, M. M., Renn, S. C. P., Shumway, C. A. and Hofmann, H. A. (2007). Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain Behav. Evol. 70, 21-39.
72. R Development Core Team (2006). R:A language and environment for statistical computing. R. Foundation for Statistical Computing, Vienna, Austria. 〈http://www.R-project.org〉
73. Redies, C. and Puelles, L. (2001). Modularity in vertebrate brain development and evolution. BioEssays 23, 1100-1111.
74. Renn, S. C. P., Aubin-Horth, N. and Hofmann, H. A. (2004). Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics 5, 42.
75. Rhodes, J. S. and Crabbe, J. C. (2005). Gene expression induced by drugs of abuse. Curr. Opin. Pharmacol. 5, 26-33.
76. Robinson, G. E., Grozinger, C. M. and Whitfield, C. W. (2005). Sociogenomics: Social life in molecular terms. Nat Rev. Genet. 6, 257-270.
77. Sagrillo, C. A., Grattan, D. R., McCarthy, M. M. and Selmanoff, M. (1996). Hormonal and neurotransmitter regulation of GnRH gene expression and related reproductive behaviors. Behav. Genet. 26, 241-277.
78. Salzburger, W., Mack, T., Verheyen, E. and Meyer, A. (2005). Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evol. Biol. 5, 15.
79. Salzburger, W., Renn, S. C. P., Steinke, D., Hofmann, H. A., Braasch, I. and Meyer, A. (2008). Annotation of expressed sequence tags for the East African cichlid fish species Astatotilapia burtoni and evolutionary analyses of cichlid ORFs. BMC Genomics 9, 96-110.
80. Santangelo, N. and Bass, A. H. (2006). New insights into neuropeptide modulation of aggression: field studies of arginine vasotocin in a territorial tropical damselfish. Proc. Biol. Sci. 273, 3085-3092.
81. Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science 308, 648-652.
82. Schick, R. R., Samsai, S., Zimmermann, J. P., Eberl, T., Endres, C., Schusdziarra, V. and Classen, M. (1993). Effect of galanin on food-intake in rats-involvement of lateral and ventromedial hypothalamic sites. Am. J. Physiol. 264, R355-R361.
83. Schlosser, G. and Wagner, G. P. (ed.) (2004). Modularity in Development and Evolution. Chicago: University Of Chicago Press.
84. Segal, E., Friedman Koller, D. and Regev, A. (2004). A module map showing conditional activity of expression modules in cancer. Nat. Genet. 36, 1090-1098.
85. Semsar, K. and Godwin, J. (2003). Social influences on the arginine vasotocin system are independent of gonads in a sex-changing fish. J. Neurosci. 23, 4386-4393.
86. Semsar, K. and Godwin, J. (2004). Multiple mechanisms of phenotype development in the bluehead wrasse. Hormones and Behavior 45, 345-353.
87. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B. and Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504.
88. Shaw, D. R., Ashburner, M., Blake, J. A., Baldarelli, R. M., Botstein, D., Davis, A. P., Cherry, J. M., Lewis, S., Lutz, C. M., Richardson, J. E. et al. (1999). Gene ontology: a controlled vocabulary to describe the function, biological process and cellular location of gene products in genome databases. Am. J. Hum. Genet. 65, A419.
89. Silverin, B., Baillien, M. and Balthazart, J. (2004). Territorial aggression, circulating levels of testosterone, and brain aromatase activity in free-living pied flycatchers. Horm. Behav. 45, 225-234.
90. Simerly, R. B. (2002). Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu. Rev. Neurosci. 25, 507-536.
91. Smyth, G. K., Thorne, N. P. and Wettenhall, J. (2004). LIMMA: Linear Models for Microarray Data, Version 1.6.6, User's Guide [http://bioinf.wehi.edu.au/limma/].
92. Sokal, R. R. and Rohlf, F. J. (1995). Biometry: The Principles and Practice of Statistics in Biological Research. 3rd edn. New York: W.H. Freeman.
93. Soma, K. K., Francis, R. C., Wingfield, J. C. and Fernald, R. D. (1996). Androgen regulation of hypothalamic neurons containing gonadotropin-releasing hormone in a cichlid fish: Integration with social cues. Horm. Behav. 30, 216-226.
94. Soma, K. K., Schlinger, B. A., Wingfield, J. C. and Saldanha, C. J. (2003). Brain aromatase, 5 alpha-reductase, and 5 beta-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior. J. Neurobiol. 56, 209-221.
95. Sorensen, C., Overil, O., Summers, C. H. and Nilsson, G. E. (2007). Social regulation of neurogenesis in teleosts. Brain Behav. Evol. 70, 239-246.
96. The Gene Ontology Consortium (2000). Gene ontology: tool for the unification of biology. Nat. Genet. 25, 25-29.
97. Tortorella, C., Neri, G. and Nussdorfer, G. G. (2007). Galanin in the regulation of the hypothalamic-pituitary-adrenal axis (Review). Int. J. Mol. Med. 19, 639-647.
98. Townsend, J. P. and Hartl, D. L. (2002). Bayesian analysis of gene expression levels: statistical quantification of relative mRNA level across multiple strains or treatments. Genome Biol. 3, research0071.1-0071.16.
99. Trainor, B. C. and Hofmann, H. A. (2006). Somatostatin regulates aggressive behavior in an African cichlid fish. Endocrinology 147, 5119-5125.
100. Trainor, B. C. and Hofmann, H. A. (2007). Somatostatin and somatostatin receptor gene expression in dominant and subordinate males of an African cichlid fish. Behav. Brain Res. 179, 314-320.
101. Trainor, B. C., Kyomen, H. H. and Marler, C. A. (2006). Estrogenic encounters: How interactions between aromatase and the environment modulate aggression. Front. Neuroendocrinol. 27, 170-179.
102. Trudeau, V. L., Spanswick, D., Fraser, E. J., Lariviere, K., Crump, D., Chiu, S., MacMillan, M. and Schulz, R. W. (2000). The role of amino acid neurotransmitters in the regulation of pituitary gonadotropin release in fish. Biochem. Cell Biol. 78, 241-259.
103. Volkoff, H., Canosa, L. F., Unniappan, S., Cerda-Reverter, J. M., Bernier, N. J., Kelly, S. P. and Peter, R. E. (2005). Neuropeptides and the control of food intake in fish. Gen. Comp. Endocrinol. 142, 3-19.
104. White, S. A., Bond, C. T., Francis, R. C., Kasten, T. L., Fernald, R. D. and Adelman, J. P. (1994). A 2nd gene for gonadotropin-releasing-hormone- cdna and expression pattern in the brain. Proc. Natl. Acad. Sci. USA 91, 1423-1427.
105. White, S. A., Nguyen, T. and Fernald, R. D. (2002). Social regulation of gonadotropin-releasing hormone. J. Exp. Biol. 205, 2567-2581.
106. Whitehead, A. and Crawford, D. L. (2006). Variation within and among species in gene expression: raw material for evolution. Mol. Ecol. 15, 1197-1211.
107. Whitfield, C. W., Cziko, A. M. and Robinson, G. E. (2003). Gene expression profiles in the brain predict behavior in individual honey bees. Science 302, 296-299.
108. Wiesenfeldhallin, Z., Xu, X. J., Langel, U., Bedecs, K., Hokfelt, T. and Bartfai, T. (1992). Galanin-mediated control of pain-enhanced role after nerve injury. Proc. Natl. Acad. Sci. USA 89, 3334-3337.
109. Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R. and Insel, T. R. (1993) A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365, 545-548.
110. Wolf, D. M. and Arkin, A. P. (2003). Motifs, modules and games in bacteria. Curr. Opin. Microbiol. 6, 125-134.
111. Wu, H., Kerr, M. K., Cui, X. and Churchill, G. A. (2002). MAANOVA: a software package for the analysis of spotted cDNA microarray experiments. In The Analysis of Gene Expression Data: Methods and Software (ed. G. Parmigiani, E. S. Garett, R. A. Irizarry and S. L. Zeger), pp. 313-341. New York: Springer-Verlag.
112. Yu, K. L. and Peter, R. E. (1991). Changes in brain levels of gonadotropin-releasing-hormone and serum levels of gonadotropin and growth-hormone in goldfish during spawning. Can. J. Zool. 69, 182-188.