sex differentiation; sex reversal; tilapia; aggressive behaviour; androgen; oestrogen
Abstract :
[en] In Nile tilapia Oreochromis niloticus, phenotypic males and females with different sexual genotypes (XX, XY, YY) have particular behavioural and physiological traits. Compared to natural XX females and XY males, XY and YY females, and XX males expressed higher level of aggressiveness that could be related to higher levels of 17β-oestradiol and 11-ketotestosterone respectively. Our results suggest that the presence of a Y chromosome increases aggressiveness in females. However, since the same relationship between aggressiveness and the Y chromosome is not observed in males, we can hypothesize that the differences in aggressiveness are not directly dependent on the genotype but on the sex reversal procedures applied on young fry during their sexual differentiation to produce these breeders. These hormonal treatments could have permanently modified the development of the brain and consequently influenced the behaviour of adults independently of their genotype. In both hypotheses (genotype or sex reversal influence), the causes of behavioural modifications have to be searched in an early modification of the brain sexual differentiation.
Disciplines :
Zoology
Author, co-author :
Gennotte, Vincent ; Université de Liège > Centre de formation et de recherche en aquaculture (CEFRA)
Akonkwa, Balagizi; Official University of Bukavu > Laboratory of Hydrobiology
Mélard, Charles ; Université de Liège > Centre de formation et de recherche en aquaculture (CEFRA)
Denoël, Mathieu ; Université de Liège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Cornil, Charlotte ; Université de Liège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Rougeot, Carole ; Université de Liège > Centre de formation et de recherche en aquaculture (CEFRA)
Language :
English
Title :
Do sex reversal procedures differentially affect agonistic behaviors and sex steroid levels depending on the sexual genotype in Nile tilapia?
Publication date :
2017
Journal title :
Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology
ISSN :
1932-5223
eISSN :
1932-5231
Publisher :
John Wiley & Sons, Hoboken, United States - New Jersey
Volume :
327
Issue :
4
Pages :
153-162
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture ARES CCD - Académie de Recherche et d'Enseignement Supérieur. Coopération au Développement
Almeida, O., Canario, A. V., & Oliveira, R. F. (2014). Castration affects reproductive but not aggressive behaviour in a cichlid fish. General and Comparative Endocrinology, 207, 34–40.
Baerends, G. P., & Baerends-van Roon, J. M. (1950). An introduction to the study of the ethology of the cichlid fishes. Behaviour, 1, 1–242.
Baroiller, J. F., & D'Cotta, H. (2001). Environment and sex determination in farmed fish. General and Comparative Endocrinology C, 130, 399–409.
Baroiller, J. F., & Jalabert, B. (1989). Contribution of research in reproductive physiology to the culture of tilapias. Aquatic Living Resources, 2, 105–116.
Billy, A. J., & Liley, N. R. (1985). The effects of early and late androgen treatments on the behaviour of Sarotherodon mossambicus (Pisces: Cichlidae). Hormones and Behavior, 19, 311–330.
Blázquez, M., & Somoza, G. M. (2010). Fish with thermolabile sex determination (TSD) as models to study brain sex differentiation. General and Comparative Endocrinology, 166, 470–477.
Boscolo, C. N. P., Morais, R. N., & Gonçalves-de-Freitas, E. (2011). Same-sized fish groups increase aggressive interaction of sex-reversed males Nile tilapia GIFT strain. Applied Animal Behaviour Science, 135, 154–159.
Carvalho, T. B., & Gonçalves-de-Freitas, E. (2008). Sex group composition, social interaction, and metabolism in the fish Nile tilapia. Brazilian Journal of Biology, 68, 807–812.
Colman, J. R., Baldwin, D., Johnson, L. L., & Scholz, N. L. (2009). Effects of the synthetic oestrogen, 17α-ethinylestradiol, on aggression and courtship behaviour in male zebrafish (Danio rerio). Aquatic Toxicology, 91, 346–354.
Cooke, B., Hegstrom, C. D., Villeneuve, L. S., & Breedlove, S. M. (1998). Sexual differentiation of the vertebrate brain: principles and mechanisms. Frontiers in Neuroendocrinology, 19, 323–362.
Desprez, D., & Mélard, C. (1998). Influence of sexual genotype on reproductive traits of females (genotype WZ) and pseudofemales (genotype ZZ) in the tilapia Oreochromis aureus. Aquatic Living Resources, 11, 145–153.
Devlin, R. H., & Nagahama, Y. (2002). Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture, 208, 191–364.
Diotel, N., Do Rego, J. L., Anglade, I., Vaillant, C., Pellegrini, E., Vaudry, H., & Kah, O. (2011). The brain of teleost fish, a source, and a target of sexual steroids. Frontiers in Neuroscience, 5, 137.
Diotel, N., Page, Y. L., Mouriec, K., Tong, S. K., Pellegrini, E., Vaillant, C.,.. Kah, O. (2010). Aromatase in the brain of teleost fish: expression, regulation and putative functions. Frontiers in Neuroendocrinology, 31, 172–192.
Douxfils, J., Mandiki, R., Silvestre, F., Bertrand, A., Leroy, D., Thomé, J. P., & Kestemont, P. (2007). Do sewage treatment plant discharges substantially impair fish reproduction in polluted rivers? Science of the Total Environment, 372, 497–514.
Falter, U. (1983). Les comportements agonistiques de Sarotherodon niloticus (Pisces: Cichlidae) et la signification évolutive de l'incubation buccale. Bulletin de la Classe des Sciences, Academie Royale de Belgique, LXIX, 566–594.
Fitzpatrick, J. L., Henry, J. C., Liley, N. R., & Devlin, R. H. (2005). Sperm characteristics and fertilization success of masculinized coho salmon (Oncorhynchus kisutch). Aquaculture, 249, 459–468.
Francis, R. C. (1992). Sexual lability in teleosts: developmental factors. Quarterly Review of Biology, 67, 1–18.
Gatewood, J. D., Wills, A., Shetty, S., Xu, J., Arnold, A. P., Burgoyne, P. S., & Rissman, E. F. (2006). Sex chromosome complement and gonadal sex influence aggressive and parental behaviours in mice. Journal of Neuroscience, 26, 2335–2342.
Geffen, A. J., & Evans, J. P. (2000). Sperm traits and fertilization success of male and sex-reversed female rainbow trout (Oncorhynchus mykiss). Aquaculture, 182, 61–72.
Gennotte, V., Francois, E., Rougeot, C., Ponthier, J., Deleuze, S., & Melard, C. (2012). Sperm quality analysis in XX, XY and YY males of the Nile tilapia (Oreochromis niloticus). Theriogenology, 78, 210–217.
Godwin, J. (2010). Neuroendocrinology of sexual plasticity in teleost fishes. Frontiers in Neuroendocrinology, 31, 203–216.
Gutzke, W. H. N., & Crews, D. (1988). Embryonic temperature determines adult sexuality in a reptile. Nature, 332, 832–834.
Haller, J. (2013). The neurobiology of abnormal manifestations of aggression: a review of hypothalamic mechanisms in cats, rodents, and humans. Brain Research Bulletin, 93, 97–109.
Huffman, L. S., O'Connell, L. A., & Hofmann, H. A. (2013). Aromatase regulates aggression in the African cichlid fish Astatotilapia burtoni. Physiology and Behavior, 112–113, 77–83.
Kwon, J. Y., McAndrew, B. J., & Penman, D. J. (2002). Treatment with an aromatase inhibitor suppresses high-temperature feminization of genetic male (YY) Nile tilapia. Journal of Fish Biology, 60, 625–636.
Laredo, S. A., Villalon Landeros, R., & Trainor, B. C. (2014). Rapid effects of estrogens on behavior: Environmental modulation and molecular mechanisms. Frontiers in Neuroendocrinology, 35, 447–458.
Li, H., Holleley, C. E., Elphick, M., Georges, A., & Shine, R. (2016). The behavioural consequences of sex reversal in dragons. Proceedings of the Royal Society B: Biological Sciences, 283, 20160217.
Liu, S., Govoroun, M., D'Cotta, H., Ricordel, M. J., Lareyre, J. J., McMeel, O. M., … Guiguen, Y. (2000). Expression of cytochrome P45011β (11β-hydroxylase) gene during gonadal sex differentiation and spermatogenesis in rainbow trout, Oncorhynchus mykiss. Journal of Steroid Biochemistry and Molecular Biology, 75, 291–298.
Longrie, N., Poncin, P., Denoël, M., Gennotte, V., Delcourt, J., & Parmentier, E. (2013). Behaviours associated with acoustic communication in Nile tilapia (Oreochromis niloticus). PLoS ONE, 8, e61467.
MacLusky, N., & Naftolin, F. (1981). Sexual differentiation of the central nervous system. Science, 211, 1294–1302.
Munakata, A., & Kobayashi, M. (2010). Endocrine control of sexual behaviour in teleost fish. General and Comparative Endocrinology, 165, 456–468.
O'Connell, L. A., Ding, J. H., & Hofmann, H. A. (2013). Sex differences and similarities in the neuroendocrine regulation of social behaviour in an African cichlid fish. Hormones and Behavior, 64, 468–476.
Oliveira, R. F., Carneiro, L. A., & Canario, A. V. M. (2005). Behavioural endocrinology: no hormonal response in tied fights. Nature, 437, 207–208.
Oliveira, R. F., & Gonçalves, D. M. (2008). Hormones and social behaviour of teleost fish. In C. Magnhagen, V. A. Braithwaite, E. Forsgren, & B. G. Kapoor (Eds.), Fish behaviour (pp. 61–150). Enfield, NH: Science Publishers Inc.
Oliveira, R. F., Hirschenhauser, K., Carneiro, L. A., & Canario, A. V. M. (2002). Social modulation of androgen levels in male teleost fish. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 132, 203–215.
Ovidio, M., Desprez, D., Mélard, C., & Poncin P. (2002). Influence of sexual genotype on the behaviour of females (genotype WZ) and pseudofemales (genotype ZZ) in the tilapia Oreochromis aureus. Aquatic Living Resources, 15, 163–167.
Pandian, T. J., & Sheela, S. G. (1995). Hormonal induction of sex reversal in fish. Aquaculture, 138, 1–22.
Paul-Prasanth, B., Bhandari, R. K., Kobayashi, T., Horiguchi, R., Kobayashi, Y., Nakamoto, M., … Nagahama, Y. (2013). Estrogen oversees the maintenance of the female genetic program in terminally differentiated gonochorists. Science Reports, 3, 2862.
Popma, T., & Masser, M. 1999. Tilapia life history and biology. SRAC Publication No. 283, Southern Regional Aquaculture Center, United States Department of Agriculture, Stoneville, Mississippi.
Rougeot, C., Nicayenzi, F., Mandiki, S. N. M., Rurangwa, E., Kestemont, P., & Mélard, C. (2004). Comparative study of the reproductive characteristics of XY male and hormonally sex-reversed XX male Eurasian perch, Perca fluviatilis. Theriogenology, 62, 790–800.
Saaristo, M., Craft, J. A., Lehtonen, K. K., & Lindström, K. (2010). Exposure to 17α-ethinyl estradiol impairs courtship and aggressive behaviour of male sand gobies (Pomatoschistus minutus). Chemosphere, 79, 541–546.
Saunders, P. A., Perez, J., Rahmoun, M., Ronce, O., Crochet, P. A., & Veyrunes, F. (2014). XY females do better than the XX in the African pygmy mouse, Mus minutoides. Evolution, 68, 2119–2127.
Siegel, S., & Castellan N, J. (1988). Nonparametric statistics for the behavioral sciences (2nd ed.). New York: McGraw-Hill.
Söffker, M., & Tyler, C. R. (2012). Endocrine disrupting chemicals and sexual behaviours in fish a critical review on effects and possible consequences. Critical Reviews in Toxicology, 42, 653–668.
Soma, K. K., Sullivan, K. A., Tramontin, A. D., Saldanha, C. J., Schlinger, B. A., & Wingfield, J. C. (2000). Acute and chronic effects of an aromatase inhibitor on territorial aggression in breeding and nonbreeding male song sparrows. Journal of Comparative Physiology A, 186, 759–769.
Summers, C. H., Korzan, W. J., Lukkes, J. L., Watt, M. J., Forster, G. L., Øverli, Ø, … Greenberg, N. (2005). Does serotonin influence aggression? Comparing regional activity before and during social interaction. Physiological and Biochemical Zoology, 78, 679–694.
Tacon, P., Baroiller, J. F., Le Bail, P. Y., Prunet, P., & Jalabert, B. (2000). Effect of egg deprivation on sex steroids, gonadotropin, prolactin, and growth hormone profiles during the reproductive cycle of the mouthbrooding cichlid fish Oreochromis niloticus. General and Comparative Endocrinology, 117, 54–65.
Toguyeni, A., Fauconneau, B., Boujard, T., Fostier, A., Kuhn, E. R., Mol, K. A., & Baroiller, J. F. (1997). Feeding behaviour and food utilisation in tilapia, Oreochromis niloticus: effect of sex ratio and relationship with the endocrine status. Physiology and Behavior, 62, 273–279.
Toguyeni, A., Fauconneau, B., Fostier, A., Abucay, J., Mair, G., & Baroiller, J. F. (2002). Influence of sexual phenotype and genotype, and sex ratio on growth performances in tilapia, Oreochromis niloticus. Aquaculture, 207, 249–261.
Tsai, C. L., & Wang, L. H. (1998). Effects of gonadal steroids on the noradrenergic activity in the early developing tilapia brain. Biogenic Amines, 14, 591–598.
Tsai, C. L., & Wang, L. H. (1999). Effects of gonadal steroids on the serotonin synthesis and metabolism in the early developing tilapia brain. Neuroscience Letters, 264, 45–48.
Tsai, C. L., Wang, L. H., Chang, C. F., & Kao, C. C. (2000). Effects of gonadal steroids on brain serotonergic and aromatase activity during the critical period of sexual differentiation in tilapia, Oreochromis mossambicus. Journal of Neuroendocrinology, 12, 894–898.
Volff, J. N., Nanda, I., Schmid, M., & Schartl, M. (2007). Governing sex determination in fish: regulatory putsches and ephemeral dictators. Sex Dev, 1, 85–99.
Vosges, M., Le Page, Y., Chung, B. C., Combarnous, Y., Porcher, J. M., Kah, O., & Brion, F. (2010). 17α-Ethinylestradiol disrupts the ontogeny of the forebrain GnRH system and the expression of brain aromatase during early development of zebrafish. Aquatic Toxicology, 99, 479–491.
Wang, L. H., & Tsai, C. L. (1999). Effects of gonadal steroids on the GABA and glutamate contents of the early developing tilapia brain. Developmental Brain Research, 114, 273–276.
Wilson, C. A., & Davies, D. C. (2007). The control of sexual differentiation of the reproductive system and brain. Reproduction, 133, 331–359.
Winberg, S., & Nilsson, G. E. (1993). Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions, with particular reference to fish. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 106, 597–614.
Zohar, Y., Munoz-Cueto, J. A., Elizur, A., & Kah, O. (2010). Neuroendocrinology of reproduction in teleost fish. General and Comparative Endocrinology, 165, 438–455.