Inhibition of cytochrome p450 brain aromatase reduces two male specific sexual behaviours in the male Endler guppy (Poecilia reticulata)

Hallgren, Stefan; Linderoth, Maria; Olsén, K. Håkan

doi:10.1016/j.ygcen.2006.02.005

Cited by 78 publications

(39 citation statements)

References 38 publications

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“…Forlano and Bass, 2005a). In a study in guppies where aromatase was pharmacologically inhibited, the frequency of male sexual displays decreased (Hallgren et al, 2006), suggesting a parallel with what has been described for birds and mammals, where the local aromatization of testosterone (T) into estradiol (E 2 ) mediates the expression of some male sexual displays (e.g. Adkins et al, 1980;Vagell and McGinnis, 1997).…”

Section: Introductionmentioning

confidence: 56%

Brain and gonadal aromatase activity and steroid hormone levels in female and polymorphic males of the peacock blenny Salaria pavo

Gonçalves

Teles

Alpedrinha

et al. 2008

Hormones and Behavior

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In the peacock blenny Salaria pavo large males with well-developed secondary sexual characters establish nests and attract females while small "sneaker" males mimic female sexual displays in order to approach the nests of larger males and parasitically fertilize eggs. These alternative reproductive tactics are sequential, as sneakers irreversibly switch into nesting males. This transition involves major morphologic and behavioral changes and is likely to be mediated by hormones. This study focuses on the role of aromatase, an enzyme that catalyses the conversion of androgens into estrogens, in the regulation of male sexual polymorphism in S. pavo. For this, sex steroid plasma levels and aromatase activity (AA) in gonads, whole brain and brain macroareas were determined in sneakers, transitional males (i.e. sneakers undergoing the transition into nesting males), nesting males and females collected in the field. AA was much higher in ovarian tissue than in testicular tissue and accordingly circulating estradiol levels were highest in females. This supports the view that elevated AA and estradiol levels are associated with the development of a functional ovary. Transitional males are in a non-reproductive phase and had underdeveloped testes when compared with sneakers and nesting males. Testicular AA was approximately 10 times higher in transitional males when compared with sneakers and nesting males, suggesting high AA has a suppressive effect on testicular development. Nesting males had significantly higher plasma levels of both testosterone (T) and 11-ketotestosterone when compared with the other male morphs and previous studies demonstrated that these androgens suppress female-like displays in sneakers. In the brain, AA was highest in macroareas presumably containing hypothalamic nuclei traditionally associated with the regulation of reproductive behaviors. Overall, females presented the highest levels of brain AA. In male morphs AA increased from sneakers, to transitional males, to nesting males in all brain macroareas. These results suggest that the transition into the nesting male tactic is accompanied both by an increase in testicular androgen production and by a higher conversion of androgens into estrogens in the brain. The increase in androgen production is likely to mediate the development of male secondary sexual characters while the increase in brain AA may be related to the behavioral changes associated with tactic transition.

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Section: Introductionmentioning

confidence: 56%

Brain and gonadal aromatase activity and steroid hormone levels in female and polymorphic males of the peacock blenny Salaria pavo

Gonçalves

Teles

Alpedrinha

et al. 2008

Hormones and Behavior

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“…In mammals, it has been shown that the conversion of androgens to estrogens in the brain is essential for brain sexual differentiation toward male pattern and activation of male sexual behavior (Lephart 1996, Balthazart & Ball 1998. In male Poecilia reticulate, a teleost fish, inhibition of cytochrome p450 brain aromatase reduced two malespecific sexual behaviors (Hallgren et al 2006). In this context, it can be hypothesized that the increased expression of cyp19a1b in the hypothalamus at the IE phase may play a role in masculinizing the brain of the ricefield eel during sex change from female to male, which awaits further study.…”

Section: Discussionmentioning

confidence: 99%

Two cytochrome P450 aromatase genes in the hermaphrodite ricefield eel Monopterus albus: mRNA expression during ovarian development and sex change

Zhang

Yang

et al. 2008

Journal of Endocrinology

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Previously, the ricefield eel (Monopterus albus) was speculated to have only one cytochrome p450 aromatase gene. In this study, however, the cDNAs encoding two distinct cytochrome p450 aromatases, cyp19a1a and cyp19a1b, were isolated. The genomic organizations of both cyp19 genes were conserved when compared with other teleosts. Northern blot detected an abundant expression of cyp19a1a in the ovary, and cyp19a1b in the hypothalamus. RT-PCR coupled with Southern blot showed that cyp19a1a was expressed predominantly in the gonads of both sexes, with higher levels in the ovary than testis, while cyp19a1b was expressed in all the tissues examined in the male, but only in the brain and pituitary in the female. The levels of cyp19a1a mRNA in the ovary were increased significantly during vitellogenesis, but decreased significantly at mature stage. The levels of cyp19a1b mRNA in the brain and pituitary did not vary significantly during vitellogenesis. As ovarian development shifted from vitellogenesis to maturation, the levels of cyp19a1b mRNA was decreased significantly in the brain, but increased significantly in the pituitary. During natural sex change from female to male, the levels of cyp19a1a mRNA in the gonad were significantly decreased. The levels of cyp19a1b mRNA in the hypothalamus were significantly increased at the early intersexual phase, whereas the expression levels in the pituitary were significantly decreased at the intersexual phases. Taken together, these results showed a novel sexual dimorphism of cyp19a1b mRNA tissue distribution, and both CYP19 genes were associated with the ovarian development and natural sex change of the ricefield eel.

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“…An experimental study testing the effects of aromatization in male guppy sexual displays found a significant decrease of these behaviors with aromatase blockage (Hallgren et al, 2006), and E 2 promoted within minutes male approach behavior towards females in the goldfish (Lord et al, 2009). On the contrary, in five studies where E 2 was administered to males, sexual displays were reduced in four cases and remained unchanged in one and similar findings have been described for fish exposed to other estrogen and estrogenic-like compounds (e.g., Colman et al, 2009).…”

Section: Differences Between Populationsmentioning

confidence: 99%

“…Studies conducted so far investigating the role of aromatization in male fish reproductive behavior have produced conflicting results (Munakata and Kobayashi, 2009). For example, in a study on guppies, aromatase activity was pharmacologically inhibited with the drug fadrozole, administered in the water, and the frequency of two of three male sexual displays decreased (Hallgren et al, 2006). Also, in the goldfish testosterone (T) and estradiol (E 2 ) injections in males stimulated approach behavior toward females within minutes, while fadrozole blocked the stimulatory effect of T (Lord et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Brain aromatase mRNA expression in two populations of the peacock blenny Salaria pavo with divergent mating systems

Gonçalves

Saraiva

Teles

et al. 2010

Hormones and Behavior

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Keywords:Aromatase Reproductive behavior Salaria pavo Peacock blenny Alternative reproductive tactics Sex-role reversal Aromatase, the key enzyme in the conversion of androgens to estrogens, regulates the availability of these hormones in tissues and controls many physiological and behavioral processes. In fish and other vertebrates, the regulation of aromatase expression in the brain has been implicated in the modulation of male sexual and aggressive behaviors. Here, the pattern of mRNA expression of the brain aromatase isoform (encoded by the CYP19A2 gene also referred as CYP19b) was quantified at the peak of spawning season in brain macroareas from males and females of the blenny Salaria pavo originated from two populations displaying male alternative reproductive tactics but differing in their mating systems. In Trieste (Adriatic) nesting males aggressively defend nests and take the initiative in courtship and perform sexual displays more often than females while in Ria Formosa (Southern Portugal) the pattern is reversed as a result of shortage of appropriate nesting sites. Nesting males from Ria Formosa had overall higher levels of brain aromatase mRNA expression than nesting males from Trieste, suggesting a higher brain estrogen synthesis in these males. Since in some fish species exogenous estradiol administration has been shown to decrease sexual and agonistic behaviors, the higher levels of brain aromatase in Ria Formosa nesting males may explain their reduced expression of sexual and aggressive displays when compared with nesting males from Trieste. Alternatively, the higher brain aromatase levels in nesting males from Ria Formosa could be a mechanism to decrease the putative androgen-induced activation of aggressive and sexual displays by reducing the local availability of androgens through their metabolization into estrogens. Although females and parasitic female-like males also differ in their displays between populations, the interpopulational pattern of brain aromatase mRNA expression was similar, suggesting that other neuroendocrine agents mediate the expression of female and female-like behaviors. In conclusion, brain aromatase availability seems like a probable mechanism to regulate the effects of steroids on the brain circuits underlying the expression of sexual and agonistic displays in S. pavo.

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Inhibition of cytochrome p450 brain aromatase reduces two male specific sexual behaviours in the male Endler guppy (Poecilia reticulata)

Cited by 78 publications

References 38 publications

Brain and gonadal aromatase activity and steroid hormone levels in female and polymorphic males of the peacock blenny Salaria pavo

Brain and gonadal aromatase activity and steroid hormone levels in female and polymorphic males of the peacock blenny Salaria pavo

Two cytochrome P450 aromatase genes in the hermaphrodite ricefield eel Monopterus albus: mRNA expression during ovarian development and sex change

Brain aromatase mRNA expression in two populations of the peacock blenny Salaria pavo with divergent mating systems

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