The saddleback wrasse, Thalassoma duperrey, inhabits corals reefs in the Hawaiian Islands. Remarkably, when the ratio of males to females in a population of wrasse becomes too low, the largest female transforms herself into a male over a 6–8-week period. Unsurprisingly, sex reversal in fishes requires a complete reorganization of physical, physiological and behavioural systems. In addition, sex reversal requires the conversion of external social cues into internal chemical cues. While past studies had investigated the roles of various hormones, neurotransmitters and neuromodulators as the trigger for the sex reversal process, an important group of chemicals that had not yet been investigated were the monoamine neurotransmitters such as dopamine, serotonin and noradrenaline. The hypothesis of the study by Larson and coworkers was that sex reversal in the wrasse would be accompanied by changes in the activities of these monoamines within different brain regions.
In order to induce sex reversal in the larger fish and investigate the role of monoamines in the process, a series of floating enclosures were set up and a large and small female were placed in each. The team chose to monitor regions of the brain that are known to be involved in regulating sexual function and behaviour and are homologous to mammalian systems. The team sampled brains from the larger fish at various time points throughout the process of sex reversal and measured the monoamine levels using high-performance liquid chromatography (HPLC).
Larson and colleagues found changes in monoamine metabolism in all of the brain regions that were examined. The most prevalent alterations in monoamine system activation were observed during the first week of sex reversal, at which time the sexual transition is primarily behavioural.
One of the brain regions sampled appeared to be involved in regulating the fish's physical alterations. In the preoptic area of the brain, linked with male sexual function and behaviour in all vertebrates, the team found changes in both serotonergic activity and noradrenergic activity, which could potentially trigger the reorganization of the reproductive axis.
The remaining four regions of the brain appeared to be involved in altering the female's behaviour during her sexual transition. The amygdala, an area in the brain that is important with respect to aggression, dominance and stress in vertebrates, exhibited significant changes in serotonin metabolism during sex reversal in wrasse. These changes were probably related to the observable increase in territorial acquisition and defense as the wrasse changed from female to male. In the ventral hypothalamus, noradrenergic activity, which is typically associated with female behaviour in this region of the brain, was reduced. By contrast, the locus coeruleus showed an increase in noradrenergic activity in the later stages of sex reversal, probably in response to an increase in circulating male sex hormones such as testosterone. The raphe nucleus showed an increase in serotonergic activity at the early, behavioural stages of sex reversal. During this time it is critical for the changing female to show dominance over other females, and dominant behaviour results in lower serotonergic activity in many animal models.
The present study is the first to investigate monoamines and their role in environmentally stimulated sex reversal and has revealed that monoamines in different brain regions are important in both behavioural and gonadal sex reversal in the saddleback wrasse.
- © The Company of Biologists Limited 2003