Neuroendocrine Transduction of Social Cues in the Bluehead Wrasse, Thalassoma bifasciatum
Understanding behavioral adaptations to changing social conditions is a key challenge for social neuroscience. The bluehead wrasse, Thalassoma bifasciatum, is a protogynous sex-changing fish with sex and role change under social control, making it an excellent system in which to study neuroendocrine mechanisms regulating male sociosexual behavior. The behavioral changes associated with a change in social dominance in bluehead wrasses are dramatic, take place rapidly, and can be studied in the full complexity of the natural environment.
Sex hormones play key roles in neural modulation of behavioral processes. Because of the likelihood of complex interplay between estrogens and androgens in the brain, steroidogenic enzymes have received much attention recently and this is especially true of the enzyme aromatase. Aromatase is responsible for the conversion of androgens into estrogens and is strongly implicated in the development and regulation of sexual behaviors in many species. In this project, we have exploited aromatase?s key role in regulating the reproductive neuroendocrine axis in order to begin investigating how changes in local estrogen synthesis are involved in the neural modifications that lead to the assumption of male-typical sexual behavior. The following studies address the neuroanatomical potential for interactions, the existence of neural sex differences in distribution, and finally the consequences of estrogen manipulations on the behavioral and neural phenotypes.
We used immunocytochemistry (ICC) to characterize distributions of aromatase-immunoreactive (ir) cells in the brain of the bluehead wrasse and to examine their relationship with AVT-ir neurons and tyrosine hydroxylase-ir (TH-ir) neurons in key sensory and integrative areas. Aromatase-ir appeared to be expressed in glial cell populations 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 and were also co-regionalized with TH-ir neurons, indicating the potential for functional interactions.
We then examined levels of brain aromatase mRNA across phenotypes of the bluehead wrasse using oligonucleotide in situ hybridization to assess sexual dimorphisms in expression. Aromatase mRNA abundances in the preoptic area of the hypothalamus were significantly higher in females compared than either initial phase (IP) males or terminal phase (TP) males. Levels in IP males were also two-fold higher than aromatase levels in TP males.
Finally, in field experiments involving gonadally-intact and gonadectomized females, we found that estradiol (E2) implants prevented behavioral sex change in large females after removal of the dominant males. By contrast, cholesterol-implanted control females showed full behavioral sex change, along with a higher frequency of aggressive interactions and male-typical courtship displays than E2-implanted animals. Following the field studies, we assessed relative abundances of aromatase mRNA and found greater expression in the POA of E2-implanted females than in cholesterol-implanted controls in gonadally-intact females.
The findings presented here are consistent with a model of estrogenic inhibition of male-typical behavior and behavioral sex change in the bluehead wrasse. Supporting evidence includes the distribution of aromatase-ir cells in brain nuclei important in neural control of behavior, differences in aromatase expression across sexual phenotype, and the prevention of behavioral sex change by estrogen implants coupled with increased mRNA abundances. We propose that decreases in neural estrogen synthesis are responsible for the expression of male-typical sexual behavior in the bluehead wrasse. This research provides a base from which we can further explore the functional relationship between neuroendocrine traits and complex behavioral shifts in this model, offering insights into social influences on the development and maintenance of sociosexual behaviors more generally.
Advisor:Dr. John Godwin; Dr. Christina Grozinger; Dr. Jane Lubischer; Dr. Stephen Nowicki; Dr. Coby Schal
School:North Carolina State University
School Location:USA - North Carolina
Source Type:Master's Thesis
Date of Publication:12/11/2007