By Rebecca Campbell Gibbel DVM, MS
Gender and sex on the reef are protean subjects, with far more nuance and flexibility than the boring binary arrangement usually found on land. The ability to change gender is such a useful life characteristic that it has evolved independently with different mechanisms in a wide variety of marine species.
1. WHO ARE THE SWINGERS?
The ability to change sex is a surprisingly widespread characteristic among fish, particularly saltwater species. For many fish, a variety of non-genetic influences govern their sex determination while they are in their embryonic stages, unlike the situation for mammals and birds whose sex is controlled by genetics. It is also possible for some fish to experience sex reversal in maturity based on environmental and social factors. Up to 500 types of fish, or 2% of global species, have this amazing ability (Cormier, 2014). In the marine animal kingdom, alternative sex strategies are quite common- with invertebrate groups like shrimp, jellyfish and corals all exhibiting examples of creative approaches to gender.
In contrast, functional sex reversal and non-genetic sex determination are quite rare in birds and mammals. However, reptiles like turtles and alligators are more gender-adaptable since they do not even have sex chromosomes!
2. SEX CHANGE VOCABULARY TERMS – these will prove useful at cocktail parties.
Organisms like fish that change gender during their lives can be considered a type of hermaphrodite, with the ability to produce both male and female gametes expressed at different times. Moray eels, clownfish, and damselfish are examples of fish that start their lives as males and then change to females. They are known as protandrous hermaphrodites, while those that are females first are protogynous, such as the reef dwelling anthias, and parrotfish.
Amphiprion percula clownfish, in an anemone host. At the moment, one is male, and one is female.
Some gender-bending fish, like cleaner wrasses and broad-barred gobies, are bidirectional hermaphrodites that change back and forth between male and female, which must be confusing to their friends and relatives. Most fish that change sex are sequential hermaphrodites that take turns functioning as males or females, but they usually make the switch only once. Examples of this are the bluehead wrasse and ocellaris clownfish.
A few, like barred hamlets and dwarf seabasses, are simultaneous hermaphrodites, which can efficiently produce sperm and eggs at the same time, with no switching necessary! This duality is taken to an extreme by the mangrove killifish, which is such a complete hermaphrodite, that it self-fertilizes, with no sex partner needed at all! But most simultaneous hermaphrodites avoid the evolutionary faux pas of self-fertilization. To accomplish this, hamlets have alternating courting behavior. One fish will first exhibit the seductive swimming moves of a female and release eggs to be fertilized by another who is acting like a male. However, a few minutes later, the pair can switch roles and inseminate each other’s gametes in reverse. Now that’s an open relationship!
3. TRIGGERS FOR TRANSFORMATION
A variety of cues can affect a fish’s initial sexual determination, and nearly all fish have the capacity to change gender while in the embryonic stage. When a population is skewed far from its normal gender ratio, reproduction is impaired. For those fish that can perform the magic trick of adult sex reversal, a number of disparate factors can cause the switch.
CUES FOR SEX DIFFERENTIATION:
- Water pollution: Contaminants from humans can be carried long distances and still cause profound effects on fish, even when diluted. The gender ratios of wild fish become skewed in the presence of fertilizers and pesticides like Atrazine in runoff. Artificial hormones such as ethinyl estradiol, even in the tiny amounts found in sewage-contaminated water, can alter the gender of developing fish embryos (Cormier, 2014).
- Climate change and pH: As carbon emissions continue to rise from human activity, the ocean absorbs increased CO2 in the atmosphere, making it more acidic.
This is measured as a low pH, and developing fish embryos are quite sensitive to this factor, resulting in an imbalanced male-predominant population when the water is more acidic (Reddon, A. R., & Hurd, P. L., 2013).
- Environmental: Temperature frequently determines the initial sex of fish, with more embryos developing as males as the water temperature rises. Even a temperature increase of one to two degrees will change the sex ratio of wild fish populations from 1:1 to 1:3, which wreaks havoc on wild populations, reducing reproductive success (Ospina-Alvarez, N., & Piferrer, F., 2008).
- Weirdly, Wolbachia parasitic bacteria living inside the cells of their hosts cause numerous reproductive derangements in fish and insects. These widespread parasites live only within ovarian cells and employ several strategies to eliminate male cells in their hosts. Since the parasites destroy the fish’s male gametes unnecessary for their own survival, the resulting infected fish populations are heavily dominated by females (Prevot, 2015).
CUES FOR ADULT SEX REVERSAL:
- Peer pressure: Many fish live in groups with gender roles requiring a balanced sex ratio. Clownfish are examples of social fishes that live symbiotically in tight quarters with anemones. Each anemone hosts only one large female, one smaller male, and a couple of androgenous juveniles in waiting. When one member of the breeding pair dies, the surviving fish seeks a replacement companion. If the new candidate is the same gender, one of the fish will change gender and even personality, assuring that the larger one is the female with the dominant role in the relationship. (Some fierce female clownfish have even attacked sharks defensively!)
- Hierarchy: In contrast, the gender situation is reversed in some fish that live in harem-like arrangements. In this case, if the dominant male dies, a succession is triggered, and a female changes her sex to take over as a male.
- Life cycle: For Caribbean parrotfish, sex reversal is normal development. Most young parrotfish start maturing as females, then changing sex as they age, becoming “terminal males.” The different stages accompany a series of color changes, making parrotfish identification particularly challenging for biology students. The timing of the sex change is cued by factors such as population density, the individual’s growth, and the mortality of community members.
Three androgynous juvenile stoplight parrotfish (Sparisoma viride) on the left, the initial phase in the center (usually female), and the terminal phase on the right (male). Coloration generally changes with the sex, and once the fish has transitioned to a terminal male, he does not revert back to female.
4. PHYSIOLOGIC MECHANISMS, or how exactly do they do it?
Now that we have explored the cues to changing sex, we will talk about how this is done. In their extended time on earth, fish have evolved diverse sex-determining approaches. Some of their solutions are anatomic, some are chemical, and some just seem hard to believe!
PHYSICAL EQUIPMENT:
Many species of sequentially hermaphroditic fish conveniently have both male and female gonads, just waiting for activation from hormonal signals. Other hermaphrodites have the gonads of just one gender and completely replace them with new sex organs of the opposite sex when they go through a sex reversal, which is an energetically costly strategy. External changes, such as new coloration and even a new body shape, may also occur..
A dramatic example of such an alteration is seen with the Asian sheepshead wrasse, Semicossyphus reticulatus. When one of these fish switches from female to male after several months in seclusion, the transitioned fish emerges larger, sporting an imposing bulbous forehead, a new pair of testes, and an aggressive nature. In the photo below, it is not hard to guess that the new male is on the right, and the female is on the left, looking somewhat wary.
HORMONES:
As with other animals, estrogen and testosterone in fish tip the balance toward male or female phenotypes. In parrotfish, which are protogynous (remember that word?), the males have high levels of testosterone, the females have high levels of estrogen, and those that are undergoing a sex change have elevated levels of a special hormone identified as 11-ketetestosterone (Cardwell and Liley, 1991).
BUT WHAT CONTROLS THE HORMONES? AROMATASE DOES!
In fish, aromatase is a versatile enzyme that governs the sex hormones, turning androgens into estrogens, which changes male gonads into ovaries. When the enzyme activity is suppressed, masculinization of the fish occurs. Aromatase is the ringmaster of the fish sex change circus! The factors that elicit sex determination- changes in water pH and temperature, chemical pollutants, and the Wolbachia parasite all affect the activity of this enzyme.
5. WHY DO THEY DO IT?
Since sex reversal is a relatively widespread phenomenon on the reef, there may be different motivations for it in different situations. But overall, evolution has driven this incredible behavior because it improves reproductive success by maximizing the chance for an individual to pass on his or her genes in different environmental conditions. There are a variety of scenarios that show why the ability to change sex is so valuable.
1. Antisocial fish with few opportunities for reproduction: Fish like the coral goby, which often stay hidden because they are snacks for everyone else, may only encounter potential partners sometimes. When they do, if one partner needs to switch gender to have two different sexes in the pairing, it is useful to be a hermaphrodite! This explanation is also valid for fish living in remote locations or cramped quarters, whether or not they are introverts!
2. Size matters: The “Size Advantage Hypothesis” theorizes that fish have reproductive advantages by being different sexes while they are at different developmental sizes. For protandrous fish like the clownfish, females are more fertile when they have grown large, so it is more advantageous for them to reproduce as males when they are small and switch to females when they reach their mature size.
3. Guarding the brood: For fish that lay eggs and tend them, rather than releasing them into the water column, it is important to have a tough and dedicated parent guarding the eggs. For species with this reproductive strategy, the egg-guarding parent is usually the more aggressive male. Sequential hermaphrodite fish can lay eggs as females and switch to males to guard their progeny and territories simultaneously, which is quite efficient!
4. Playing the odds: For fish like parrotfish, the mature stage of development as a “terminal male” is fraught with competition and hostility. The younger fishes are mostly females, who are free to grow without the need to fight their competitors. Once they grow large enough, they have better odds against their competitors and switch sex to enter the ring as males.
WHATEVER WORKS FOR YOU!
Although sex reversal may seem odd from our point of view, it is actually a potent evolutionary power that results in enhanced reproductive success for species endowed with this ability. The many approaches that fish take to reproduction show us that there is not just one way of doing things!
A large family of baby fish who don’t know or care about their parents’ genders.
REFERENCES
Cardwell, J. R., & Liley, N. R. (1991). Hormonal control of sex and color change in the stoplight parrotfish, Sparisoma viride. General and Comparative Endocrinology, 81(1), 7-20. doi:10.1016/0016-6480(91)90120-U. PMID 2026318
Cormier, Z. (2014). “Fish are the sex-switching masters of the animal kingdom” Our Blue Planet. British Broadcasting System. Archived from the original on 2017012-01.
Ospina-Alvarez, N., & Piferrer, F. (2008). Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PloS one, 3(7), e2837.
Prevot, K. (2015). Wolbachia. Arizona State University. School of Life Sciences. Center for Biology and Society. Embryo Project Encyclopedia.| Arizona Board of Regents.
Reddon, A. R., & Hurd, P. L. (2013). Water pH during early development influences sex ratio and male morph in a West African cichlid fish, Pelvicachromis pulcher. Zoology, 116(3), 139-143.
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