Social Status and Neurogenomic States

Abstract

Is endocrinology at a pivotal point for integrating the effects of the social environment on plasticity in physiology and behavior through changes in gene expression? Sex steroids have a canalizing effect during early sexual differentiation, emphasizing the organizational and longlasting effects of steroid hormones. What about hormonal effects on transcriptional regulation during adulthood? Using a systems integration of endocrinology, genes, and behavior that places the organism in the context of its social environment, O’Connell and Hofmann (1) in this issue focus primarily on the role of steroid hormone receptors in the adult male African cichlid fish, Astatotilapia burtoni. In this cichlid, male behavior and reproduction are fairly canalized into either being reproductive and dominant or reproductively suppressed (small gonads) and subordinate. These differences extend into behavior and communication: the dominants are brightly colored, court and mate with females, are territorial, and chase subordinate males. The subordinates are dull in coloration and school with females. What makes this an intriguing system to work with is that the subordinate status of an individual can very rapidly switch to a dominant status (2). Some highly coordinated changes have to occur for this transition in behavior, morphology and increased androgen and estrogen levels. O’Connell and Hofmann (1) manipulate androgen receptor (AR), estrogen receptor (ER), and progestin receptor in the dominants and subordinates. They then probe the preoptic area of the brain for candidate genes regulated in either social state, with a focus on ER manipulations. These manipulations are all conducted in a stable social group. Although aggression was positively influenced by ER manipulations in both social states, only the subordinates have decreases in 17 -estradiol, testosterone, and progesterone levels in response to ER antagonists. Behavioral changes and tissue responses were therefore not parallel between the two behavioral types. This dissociation between aggressive behavior and steroid hormones has been shown in other vertebrate systems as well (3, 4). Something about the ER and associated cellular mechanisms respond differently based on changes created by the social interactions. Interestingly, subordinates were more responsive to the manipulations. It is again not parallel when the focus is on courtship, although the mechanisms likely differ; only in dominants was courtship positively associated with AR manipulations, but again, dominants showed no change in hormone levels in response to the antagonists (subordinates do not display courtship behavior). Perhaps even more revealing is that ER antagonists decreased gonad size only in subordinates within days. It is again the subordinates that are showing rapid and dramatic changes in morphology to steroid receptor manipulations even if it is not expressed in the behavior; perhaps the ER system allows subordinates to physiologically prepare for the possibility of becoming a dominant, while maintaining dissociation with the behavior. In a relatively complex social system, independent control of behavior may be important because it is the most rapid mode of communication with others of the social group, and for a subordinate, it may create an increased risk of becoming injured. In a comparison using gene expression profiling through transcriptomeanalysis, theauthors found that the preoptic area expresses 56% more genes in dominants compared with subordinates. At the level of candidate genes, ER antagonists did not alter either isomorph of AR (AR or AR ) or ER (ER a or ER b) or ER in either dominants or subordinates. The focal point of change is