[en] Social interactions can generate rapid and dramatic changes in behaviour and neuroendocrine activity. We investigated the effects of a changing social environment on aggressive behaviour and brain aromatase activity (bAA) in a sex-changing fish, Lythrypnus dalli. Aromatase is responsible for the conversion of androgen into oestradiol. Male removal from a socially stable group resulted in rapid and dramatic (>= 200%) increases in aggression in the dominant female, which will become male usually 7-10 days later. These dominant females and recently sex-changed individuals had lower bAA but similar gonadal aromatase activity (gAA) compared to control females, while established males had lower bAA than all groups and lower gAA than all groups except dominant females. Within hours of male removal, dominant females' aggressive behaviour was inversely related to bAA but not gAA. These results are novel because they are the first to: (i) demonstrate socially induced decreases in bAA levels corresponding with increased aggression, (ii) identify this process as a possible neurochemical mechanism regulating the induction of behavioural, and subsequently gonadal, sex change and (iii) show differential regulation of bAA versus gAA resulting from social manipulations. Combined with other studies, this suggests that aromatase activity may modulate fast changes in vertebrate social behaviour.
Disciplines :
Zoology Neurosciences & behavior
Author, co-author :
Black, M. P.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Baillien, M.
Grober, M. S.
Language :
English
Title :
Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex-changing fish, Lythrypnus dalli
Publication date :
22 November 2005
Journal title :
Proceedings of the Royal Society. Biological Sciences
Baillien, M. & Balthazart, J. 1997 A direct dopaminergic control of aromatase activity in the quail preoptic area. J. Steroid Biochem. Mol. Biol. 63, 99-113. (doi:10.1016/S0960-0760(97)00080-0.)
Bakker, J., Brand, T., van Ophemert, J. & Slob, A. K. 1993 Hormonal regulation of adult partner preference behavior in neonatally ATD-treated male rats. Behav. Neurosci. 107, 480-487. (doi:10.1037//0735-7044.107.3.480.)
Balthazart, J., Baillien, M., Charlier, T. D. & Ball, G. F. 2003 Calcium-dependent phosphorylation processes control brain aromatase in quail. Eur. J. Neurosci. 17, 1591-1606. (doi:10.1046/j.1460-9568.2003.02598.x.)
Black, M. P., Moore, B., Canario, A. V. M., Ford, D., Reavis, R. H. & Grober, M. S. 2005 Reproduction in context: field testing a laboratory model of socially controlled sex change in Lythrypnus dalli (Gilbert). J. Exp. Mar. Biol. Ecol. 318, 127-143.
Borg, B. 1994 Androgens in teleost fishes. Comp. Biochem. Physiol. C 109, 219-245. (doi:10.1016/0305-0491(94) 90005-1.)
Bradford, M. M. 1976 A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
Brantley, R. K., Wingfield, J. C. & Bass, A. H. 1993 Sex steroid levels in Porichthys notatus, a fish with alternative reproductive tactics, and a review of the hormonal bases for male dimorphism among teleost fishes. Horm. Behav. 27, 332-347. (doi:10.1006/hbeh.1993.1025.)
Callard, G. V. & Tchoudakova, A. V. 1997 Evolutionary and functional significance of two CYP19 genes differentially expressed in brain and ovary of goldfish. J. Steroid Biochem. Mol. Biol. 61, 387-392. (doi:10.1016/S0960- 0760(97)80037-4.)
Callard, G. V., Petro, Z. & Ryan, K. 1978 Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology 103, 2283-2290.
Carlisle, S. L. 2001 Androgens mediate changes in sexually dimorphic structures in the bluebanded goby. Master Thesis, Arizona State University, Tempe, AZ, USA.
Carlisle, S. L., Marxer-Miller, S. K., Canario, A. V. M., Oliveira, R. F., Carneiro, L. & Grober, M. S. 2000 Effects of 11-ketotestosterone on genital papilla morphology in the sex changing fish Lythrypnus dalli. J. Fish Biol. 57, 445-456. (doi:10.1006/jfbi.2000.1320.)
Contractor, R. G., Foran, C. M., Shuanfang, L. & Willett, K. L. 2004 Evidence of gender- and tissue-specific promoter methylation and the potential for ethinylestradiol-induced changes in Japanese medaka (Oryzias latipes) estrogen receptor and aromatase genes. J. Toxicol. Environ. Health A 67, 1-22.
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. (doi:10.1016/S0044-8486(02) 00057-1.)
Elbrecht, A. & Smith, R. G. 1992 Aromatase enzyme activity and sex determination in chickens. Science 255, 467-470.
Francis, R. 1992 Sexual lability in teleosts-developmental factors. Q. Rev. Biol 67, 1-18. (doi:10.1086/417445.)
Godwin, J., Crews, D. & Warner, R. R. 1996 Behavioral sex change in the absence of gonads in a coral reef fish. Proc. R. Soc. B 263, 1683-1688.
Grober, M. S. 1997 Conserved neuroendocrine foundations give rise to diverse sexual phenotypes in fish. In Sexual orientation: toward biological understanding (ed. L. Ellis & L. Ebertz), pp. 2-20. Westport, CT: Praeger.
Grober, M. S. & Bass, A. 1991 Neuronal correlates of sex/role change in labrid fishes: LHRH-like immunoreactivity. Brain Behav. Evol. 38, 302-312.
Kelly, M. J. & Ronnekleiv, O. K. 2002 Rapid membrane effects of estrogen in the central nervous system. In Hormones, brain and behavior (ed. D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrbach & R. T. Rubin), pp. 361-380. San Diego: Academic Press.
Kincl, F. A., Kramer, C. H. & Koulish, S. 1987 Sex reversal in wrasses. I. Uptake of testosterone by the gonads and central nervous system and its aromatization in the CNS of Thalassoma duperrey (Teleostei: Labridae). Endocrinol. Exp. 21, 115-123.
Kishida, M. & Callard, G. V. 2001 Distinct cytochrome P450 aromatase isoforms in zebrafish (Danio rerio) brain and ovary are differentially programmed and estrogen regulated during early development. Endocrinology 142, 740-750. (doi:10.1210/en.142.2.740.)
Kroon, F. J. & Liley, N. R. 2000 The role of steroid hormones in protogynous sex change in the blackeye goby, Coryphopterous nicholsii. Gen. Comp. Endocrinol. 118, 273-283. (doi:10.1006/gcen.2000.7459.)
Kroon, F. J., Munday, P. L., Westcott, D. A., Hobbs, J.-P. A. & Liley, N. R. 2005 Aromatase pathway mediates sex change in each direction. Proc. R. Soc. B 272, 1399-1405. (doi:10.1098/rspb.2005.3097.)
Lee, Y.-H., Yueh, W.-S., Du, J.-L., Sun, L.-T. & Chang, C.-F. 2002 Aromatase inhibitors block natural sex change and induce male function in the protandrous black porgy, Acanthopagarus schlegeli Bleeker: possible mechanism of natural sex change. Biol. Reprod. 66, 1749-1754.
Lephart, E. D. 1996 A review of brain aromatase cytochrome P450. Brain Res. Brain Res. Rev. 22, 1-26. (doi:10.1016/0165-0173(96)00002-1.)
McEwen, B. S. & Alves, S. E. 1999 Estrogen actions in the central nervous system. Endocr. Rev. 20, 279-307. (doi:10. 1210/er.20.3.279.)
Oliveira, R. F., Canario, A. V. & Grober, M. S. 2001 Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (Pisces: Blenniidae). Horm. Behav. 40, 266-275. (doi:10.1006/hbeh.2001. 1683.)
Pasmanik, M., Schlinger, B. A. & Callard, G. V. 1988 In vivo steroid regulation of aromatase and 5 alpha-reductase in goldfish brain and pituitary. Gen. Comp. Endocrinol. 71, 175-182. (doi:10.1016/0016-6480(88)90308-5.)
Pinckard, K. L., Stellflug, J., Resko, J. A., Roselli, C. E. & Stormshak, F. 2000 Review: brain aromatization and other factors affecting male reproductive behavior with emphasis on the sexual orientation of rams. Domest. Anim. Endocrinol. 18, 83-96. (doi:10.1016/S0739-7240(99)00065-X.)
Reavis, R. H. & Grober, M. S. 1999 An integrative model of sex change: social, behavioral and neurochemical changes in Lythrypnus dalli (Pisces). Acta Ethol. 2, 51-60.
Remage-Healey, L. & Bass, A. H. 2004 Rapid hierarchical modulation of vocal patterning by steroid hormones. J. Neurosci. 24, 5982-5900. (doi:10.1523/JNEUROSCI. 1220-04.2004.)
Roselli, C. E. 1991 Sex differences in androgen receptors and aromatase activity in microdissected regions of the rat brain. Endocrinology 128, 1310-1316.
Roselli, C. E. & Resko, J. A. 1991 In vitro assay of aromatase activity in the central nervous system. In Neuroendocrine research methods (ed. B. Greenstein), vol. 2, pp. 937-951. Switzerland: Harwood Academic Publishers.
Schlinger, B. A. & Arnold, A. P. 1991 Brain is the major site of estrogen synthesis in a male songbird. Proc. Natl Acad. Sci. USA 88, 4191-4194.
Schlinger, B. A., Greco, C. & Bass, A. H. 1999 Aromatase activity in the hindbrain vocal control region of a teleost fish: divergence among males with alternative reproductive tactics. Proc. R. Soc. B 266, 131-136. (doi:10.1098/rspb. 1999.0612.)
Schumacher, M. & Balthazart, J. 1986 Testosterone-induced brain aromatase is sexually dimorphic. Brain Res. 370, 285-293. (doi:10.1016/0006- 8993(86)90483-X.)
Simpson, E., Rubin, G., Clyne, C., Robertson, K., O'Donnell, L., Jones, M. & Davis, S. 2000 The role of local estrogen biosynthesis in males and females. Trends Endocrinol. Metab. 11, 184-188. (doi:10.1016/S1043-2760(00) 00254-X.)
Mary, St. C. M. 1993 Novel sexual patterns in two simultaneous hermaphroditic gobies, Lythrypnus dalli and Lythrypnus zebra. Copeia 4, 1062-1072.
Tchoudakova, A. & Callard, G. V. 1998 Identification of multiple CYP19 genes encoding different cytochrome P450 aromatase isozymes in brain and ovary. Endocrinology 139, 2179-2189. (doi:10.1210/en.139.4.2179.)
Trainor, B. C., Bird, I. M. & Marler, C. M. 2004 Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Horm. Behav. 43, 113-121.
Zhao, J., Mak, P., Tchoudakova, A., Callard, G. & Chen, S. 2001 Different catalytic properties and inhibitor responses of the goldfish brain and ovary aromatase isozymes. Gen. Comp. Endocrinol. 123, 180-191. (doi:10.1006/gcen.2001. 7661.)