Ocean Newsletter
No.567 March 20, 2024
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Marine Organisms that can Change Gender—A Gender Strategy
IWATA Eri, D.V.M., Ph.D.(Faculty of Veterinary Medicine, Okayama University of Science)
The sex determination system of marine organisms is highly diverse and different from that of human beings, who have a strong sex determination system based on XY chromosomes. Among these, multiple fish species have been reported to demonstrate gender changing attributes. Changing gender is not a rare phenomenon among fish species, and is highly logical from the viewpoint of their survival strategy.
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Boats Connecting Men and Women: Gender Perspectives on Boatbuilding in South Sulawesi
MYOJYO Tsukiko (Visiting Researcher, Research Area of Human Society, Kanazawa University)
The Bugis have historically been widely active in the Southeast Asian maritime world with their outstanding boatbuilding, sailing skills, and extensive maritime networks. They create ‘navels’ on their boats through which souls are infused. The Bugis people's houses and boats are perceived as symbolic spaces that embody their cosmology, including their gender norms and ideas of procreation.
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Coexistence of Diverse Sexualities in Polynesia ~Mahu and Raerae~
KUWAHARA Makiko (Professor, Department of International Communication, College of Humanities, Kinjo Gakuin University)
In French Polynesia in the South Pacific, even before contact with Western culture, there were people born male but took on the role of women. Since the opening of an airport in Tahiti in 1960, the society has been transformed by outside cultural influences, and the ‟raerae” have appeared in addition to the traditional “mahu”. This paper presents examples of the coexistence of diverse sexualities in the islands of Oceania.
Marine Organisms that can Change Gender—A Gender Strategy
The Social Hierarchy of Anemonefish, and Gender-changing
Anemonefish is a tropical fish that inhabits coral reefs in the Indo-Pacific tropical region. Currently, 28 species of anemonefish have been reported worldwide, six of which live in the coastal regions of the Japanese archipelago (Figure 1). Anemonefish are well known as a fish species that live symbiotically with sea anemones, but there is no genetic relationship between the species of anemonefish that live in the same sea anemone. Social hierarchy (dominance) within a school of anemonefish is formed based on size; that is, ranking within the school is determined by body length, with the largest fish being the most dominant, the second largest ranking second, the third largest ranking third, and so on.
In general, members of a school of anemonefish engage in threatening and submissive behaviors routinely and repeatedly. Such behaviors are important not only for maintaining order within the school, but also play a crucial role in their reproduction. Their gender is not determined by genetic information but by their social rank within the school. The gonads of anemonefish that have not yet reached sexual maturity contain both ovarian and testicular parts within a single organ. In the case of anemonefish, the outer part comprises immature ovarian tissue, while the inner part is made up of testicular tissue containing sperm. When the social rank of a fish within the school is established as second, its ovarian part diminishes, and the testicular part increases such that it acquires male functionality. When a fish is ranked as the most dominant in the school, the testicular part of its gonad gradually retracts, leaving only the ovarian part. The ovarian follicle matures, enabling it to function as a female (Figure 2). These are the only two fishes within the school to become a breeding pair that periodically and repeatedly spawns and releases sperm. Fishes ranked third and lower continue to possess immature hermaphrodite gonads. However, in the case of unforeseen events, such as when dominant fishes are preyed upon or swept away by a typhoon, the social rank of lower-ranking fishes is elevated. For example, if there are no females left in the school, the male anemonefish in the second rank will rise to the first rank and undergo a gender transformation to fill the female role. As a result, the fish previously ranked third will move into second place and transition from a sexually immature state to function as a male.
It is highly logical for anemonefish to possess such ecology. Anemonefish are poor swimmers, making it considerably difficult for fishes ranked third or lower to seek breeding opportunities by moving between different sea anemones. Therefore, they must wait for their chance to move up in rank within a single sea anemone. On the other hand, the same fishes that form the dominant breeding pair spawn and release sperm regularly and repeatedly. In this case, it is advantageous for the fish species if the body of the female is larger. This is because producing one yolk-rich egg is more costly than producing a single sperm. Additionally, anemonefish spawn on rocky surfaces next to sea anemones, and the male takes on the role of tending to the eggs until they hatch, such as aerating them with fresh seawater and cleaning them. While the male diligently tends to the eggs, the female focuses on eating voraciously to recover her strength in preparation for the next spawning act. In other words, anemonefish regard a school residing in a sea anemone as a single breeding unit, and they have a "social system" that enables this unit to continue with its reproduction activities.

■Figure 1: Six species of anemone that can be found in Japan

■Figure 2: Gonadal tissues of the common anemonefish (Scale: 500 μm)
Various Types of Gender changing Fish
In contrast to the anemonefish, the wrasse family undergoes gender transformation from female to male. Many wrasse species have a large, dominant male that establishes a territory and corrals multiple females to form a harem-like school. If the harem’s dominant male dies or disappears, it is known that the female in the harem with the largest physical size changes its gender to become a male. For fish species that use a harem-based reproductive strategy, it is advantageous for the male guarding the harem to have the largest and strongest body.
Furthermore, there are also fish species known to switch between male and female multiple times throughout their lifetime. One such example in Japan is the Okinawa rubble goby which inhabits rocky areas from Izu to Okinawa. When two Okinawa rubble goby encounter each other during breeding season, the larger fish becomes the male and the smaller one becomes the female, adapting their roles as needed for reproduction. The period required for this gender transformation is very short, lasting about four days. For small Okinawa rubble goby that cannot travel long distances, switching between male and female roles as necessary for efficient breeding is a highly rational method to ensure that they do not waste valuable encounters.
Apart from social hierarchy, there are also examples of gender changes due to other environmental factors besides social hierarchy. The blackhead sea bream and grouper families have hermaphrodite gonads when they are young fish, then reach sexual maturity later as females. After reaching a certain size, they are known to undergo gender transformation from female to male. In other words, their gender changes with age.
Changing Gender as a Survival Strategy
For fish species, changing their own gender as a survival strategy to ensure successful reproduction is certainly not a rare phenomenon. Currently, about 500 species of fish worldwide have been reported to undergo gender transformation after reaching sexual maturity. However, since it is difficult for humans to closely observe the behavior of all fish in the sea, it is likely that many more fish have the ability to change their gender.
Our vertebrate ancestors were fish born in the sea. Fish have developed various mechanisms for sex determination, but as they later ventured onto land and evolved, these mechanisms were refined gradually in the evolution process, leading to the establishment of a strong sex determination system based on XY chromosomes, as seen in modern-day mammals.
In fact, there are remarkably few animal species that have sex determination systems like mammals. Marine organisms, in particular, are truly fascinating. Looking across many animal species, I hope that I have communicated the fact that it is common for sexuality to be fluctuating and uncertain. (End)