Laura Casas, House of Wisdom guest blogger and King Abdullah University of Science & Technology (KAUST) marine biologist, talks to us about the orange salt water fish and how it used a marvelous evolutionary mechanism to conquer the seas.
{credit}Fran Saborido-Rey{/credit}
How did a small, very bright, colorful fish that’s a poor swimmer become extensively distributed in tropical waters from the Indian to the western Pacific Oceans, including the Great Barrier Reef and the Red Sea?
Two processes have potentially played a role in the successful evolutionary adaptation of clownfishes: a mutual relationship with anemones – flower-like marine animals and relatives to corals – which provides shelter and protection in exchange for nourishment, plus their capacity to change sex when their partner dies, preventing the need for dangerous travel across the reef.
While the different aspects of this mutual relationship have been unveiled in dozens of studies, very little has been known about the mechanisms that orchestrate sex change in fishes.
Our new study at KAUST provides insights into the genetic mechanism governing social sex change in fish, using the Red Sea endemic species of clownfish, Amphiprion bicinctus, as a model in its natural habitat.
Clownfishes are monogamous, living in social assemblages as pairs or social groups consisting of a dominant female, always the largest in size, surrounded by her male partner and a variable number of immature juveniles of smaller size. They display a strong social hierarchy based on size; these hierarchies function as queues for breeding, so when a dominant female of a social group dies, all subordinates seize the opportunity to ascend in rank.
This way, the male is always poised to become female and rapidly changes sex to assume the vacated position, while the biggest juvenile rapidly matures into a male ensuring the ability to produce new generations without abandoning the anemone.
{credit}Thamer S. Habis{/credit}
The confinement of an animal, however, is known to alter its normal behaviour but traditionally sex change has been studied using aquarium experiments. In our study, we localized sixteen families living on the exposed side of Al-Fahal reef, in the Central Red Sea and removed all the females to trigger the sex change process.
One sex-changing individual was sampled every five days for 1.5 months to cover the full time course of the sex change process and their transcriptional responses were assessed using RNA sequencing.
Our results show a response in the male´s brain which starts two weeks after the female’s disappearance and lasts for two additional weeks.
During this period, there is a marked down-regulation in deferentially expressed genes of sex-changing individuals, compared to mature males and females. We identify a large number of candidate genes, both well-known and novel potentially playing a role in sex change.
Based on our results, we propose a picture of the genetic mechanisms that take place during the sex shift: the aromatase gene known as cyp19a1 plays a central role by modulating the balance between estrogen and androgen signaling. Aromatase is involved in the production of estrogen.
The genes sox6 and foxp4 may play a role in regulating the expression of aromatase and/or other genes involved in steroid production at the brain level. The genes cyp19a1 and foxl2 play a pivotal role in the activation of the female pathway driving the sex gland transformation from testis to ovary during sex change, while Sox8, Dmrt1 and Amh are important for testis maintenance.
The results have not only provided important insight into the main genetic mechanism governing sex change and sex gland restructuring in hermaphrodite flowers or animals, but also detailed information on specific genes involved during every step of the process. Our study is the first genome-wide study in a social sex-changing species in its natural habitat and the dataset generated is a valuable genomic resource for a species with virtually no genetic information available in public datasets.
Future work would ideally explore whether the genetic processes underlying sex change in hermaphrodites is evolutionary conserved. We need to deepen our knowledge of the unexplored genetic mechanisms underlying such sex change.
As well, only a deep understanding of the genetic processes governing reproduction in hermaphrodites will allow us to anticipate how reproductive success might be affected by the temperature rise in coming years as a consequence of the climate change and give us a chance to conserve and protect the sea’s biodiversity.
