The male who used to receive orders from the female now displays aggression and dominance, beginning to court the smaller fish as the female would. Shortly after the female is removed, the behavioral repertoire switches. This ability allows the formation of a new breeding pair, preventing the need for dangerous travel across the reef, but requires the presence of subdominant fish to complete the sex change 5. The male is poised to become female and rapidly changes sex to assume the vacated position, while the largest undifferentiated fish completes the breeding pair by turning into a mature male in a short time 4, 8. If the dominant female of a family dies, all subordinates seize the opportunity to ascend in rank and grow. Although a simplification, we hereafter call these social assemblages families. In a given group, the fish age and grow larger together, with their relative size differences and the dominance hierarchies among group members remaining unchanged 10. These hierarchies function as queues for breeding. Clownfish species display a strong social hierarchy based on size 9. The sessile nature of anemones makes clownfishes a good system for investigating socially-controlled sex change since the process can be monitored in experiments conducted in the field.Ĭlownfishes live in social assemblages as pairs or social groups consisting of a dominant female, always the largest in size, surrounded by a male and a variable number of immature juveniles of smaller size 8. They live in an obligate symbiosis with certain sea anemones that provide the fish with nesting sites and protection from predators 7. However, our understanding of the molecular pathways underlying reproductive processes, particularly sex change in hermaphrodites, is very limited.Ĭlownfishes (subfamily Amphiprioninae) are extensively distributed in tropical waters, where they inhabit shallow waters across the Red Sea, the Indian and the western Pacific Oceans 6. It has been suggested that sequential hermaphroditism in reef habitats improves adaptation, increases survival rates and enhances reproduction 3. male does not change sex when attaining a certain size, but only after the female disappearance. One interesting exception are the clownfishes (subfamily Amphiprioninae) which are protandrous, monogamous and sex change seems to be controlled socially 4, 5, i.e. In territorial-haremic species sex change is socially mediated, and it is more common in protogynous species. In some, particularly in protandrous species, sex change is size dependent and eventually every fish in the population will change sex. Factors triggering sex change differ among species. In simultaneous hermaphroditism individuals possess fully functional male and female gonads while in sequential hermaphroditism fish change sex sometime during its life, either from male to female (protandry) or from female to male (protogyny). Among these, functional hermaphroditism is a unique strategy 2 that has been adopted by at least 27 families across seven orders of teleosts, mainly in the coral reef environment 3. Teleost fishes display the largest array of sex-determining systems among animals, resulting in a large number of reproductive strategies, a key factor in explaining their success during evolution 1. This work constitutes the first genome-wide study in a social sex-changing species and provides insights into the genetic mechanism governing social sex change and gonadal restructuring in protandrous hermaphrodites.
The present study provides strong evidence of the importance of the sex steroidogenic machinery during sex change in clownfish, with the aromatase gene playing a central role, both in the brain and the gonad. Our analysis has highlighted the rapid and complex genomic response of the brain associated with sex change, which is subsequently transmitted to the gonads, identifying a large number of candidate genes, some well-known and some novel, involved in the process. Our study has examined relative gene expression across multiple groups-rather than just two contrasting conditions- and has allowed us to explore the differential expression patterns throughout the whole process. Here, we provide the first de novo transcriptome analyses of a hermaphrodite teleost´s undergoing sex change in its natural environment. The reproductive biology of hermaphrodites has long been intriguing however, very little is known about the molecular pathways underlying their sex change. Sequential hermaphroditism is a unique reproductive strategy among teleosts that is displayed mainly in fish species living in the coral reef environment.
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