Estrogenic control of behavioral sex change in the bluehead wrasse, Thalassoma bifasciatum.

Estrogens activate male-typical sexual behavior in several mammalian and avian models. Estrogen signaling also appears critical in the control of sex change in some fishes, in which it is instead decreases in estradiol levels that may permit development of male-typical behaviors. The bluehead wrasse is a protogynous hermaphrodite that exhibits rapid increases in aggressive and male-typical courtship behavior as females undergo sex change. Removal of the ovaries does not prevent these changes. In two field experiments involving gonadally-intact and gonadectomized females, estradiol (E2) implants prevented behavioral sex change in large females who were made the largest members of their social groups through removals of more dominant fish. In contrast, cholesterol-implanted control females showed full behavioral sex change, along with a higher frequency both of aggressive interactions and of male-typical courtship displays than occurred in E2-implanted animals. To assess potential neural correlates of these behavioral effects of E2, we evaluated abundances of aromatase mRNA using in situ hybridization. Aromatase mRNA was more abundant in the POA of E2-implanted females than in cholesterol-implanted controls in gonadally-intact females. The lack of behavioral sex change coupled with increased levels of aromatase mRNA are consistent with an inhibitory role for E2, likely of neural origin, in regulating socially controlled sex change.

Aromatase immunoreactivity in the bluehead wrasse brain, Thalassoma bifasciatum: immunolocalization and co-regionalization with arginine vasotocin and tyrosine hydroxylase.

Sex steroid hormones regulate various neural functions that control vertebrate sociosexual behavior. A number of sex steroids can be synthesized de novo in the brain, including estrogens by the enzyme aromatase. Aromatase, the neuropeptides arginine vasotocin/vasopressin, and the monoamine neurotransmitter dopamine have all been implicated in the control of male sexual and aggressive behavior in a variety of vertebrates. This study examined the expression of brain aromatase in the bluehead wrasse (Thalassoma bifasciatum), a teleost fish that exhibits socially controlled behavioral and gonadal sex change. We used immunocytochemistry (ICC) to characterize distributions of aromatase-immunoreactive (ir) cells, and to examine their relationship with AVT-ir neurons and tyrosine hydroxylase-ir (TH-ir) neurons in key sensory and integrative areas of the brain of this species. Aromatase-ir appeared to be in glial cell populations, and was found in the dorsal and ventral telencephalon, the preoptic area of the hypothalamus, and the lateral recess of the third ventricle, among other brain areas. Aromatase-ir fibers are closely associated with AVT-ir neurons throughout the preoptic area, indicating the potential for functional interactions. Aromatase-ir cell bodies and fibers were also co-regionalized with TH-ir neurons, suggesting possible interaction between the dopaminergic system and neural estrogen production. The presence of aromatase in brain regions important in the regulation of sexual and aggressive behavior suggests that local estrogen synthesis could regulate sex change through effects on signaling systems that subserve reproductive behavior and function.