Sex in the Sea: How Sex-Changing Fish Are Biologically Advantaged

As our society becomes more accustomed to conversations about sex and gender—in terms of biology, psychology, and justice—it is becoming clear just how complex and nuanced these topics can be. While we strive to understand the details of human sexuality, many of us don’t stop to consider the bigger picture: Gender and sexual fluidity isn’t a human-specific concept. Species that walk, swim, and fly about the Earth have fascinating sex lives, some of which we’re just beginning to understand.

Dr. Marah Hardt’s research is bringing us closer to understanding the bigger picture, specifically in relation to sea life. The research director of Future of Fish—a nonprofit incubator working to solve oceanic challenges—Hardt is currently engaging with organizations to find solutions to global overfishing problems. Having spent much of her career studying life among coral reefs, she became an expert in the sex lives of certain fish and ocean creatures, eventually writing the book Sex in the Sea (St. Martin’s Press, 2016), a humorous and captivating examination of the underwater mating rituals most of us have never seen. The following excerpt dives into the world of sex-changing fish, and is from the book’s chapter “Flex Your Sex: Sex Change in the Sea.”

Once Upon a Time there was a King and Queen who ruled over a peaceful kingdom. The peace came from order, and that order was imposed through fierce intimidation. No one dared rise up to challenge their reign. Beautiful and standing a full foot taller than the King, it was no secret that the Queen was in command. It was even rumored that she bullied her King, just as he bullied his court.

Then, one night, the Queen died. Within moments, a strange new force began to swirl within the castle walls. As if released from some spell the King felt a change deep within himself, a blossoming of something new, something different, something . . . feminine. For the next few weeks this inner transformation progressed until finally he stepped forth as a new and powerful Queen, equally as beautiful, fertile, and commanding as the former had been.

The King-now-Queen took as her mate a spirited youth who had, under the same spell, developed into a strapping, virile male. Under the new Queen’s hard-hearted watch, the new King embraced his role and began a new reign of intimidation—and the two lived and laid many successful clutches of eggs, Happily Ever After.

The End.

Or so a fairy tale might go, had the Brothers Grimm known anything about clownfish. Yes, clownfish. Sorry folks, but Pixar got it wrong. Way wrong.

When it comes to relationship dynamics of clownfish, the true adventure tale reads more like the Greek tragedy Oedipus than it does Finding Nemo. As Nature writes the story, by the time Nemo hatched out of the egg, his dad, Marlin, an unpartnered male head of household, would have already morphed into Marlene. For clownfish, when the leading lady dies, the top dog promotes to bitch.

Rather than chasing after a kidnapped Nemo, Marlin-now-Marlene would stay at home and welcome the next largest male around to join her as her chosen mate inside her spacious anemone abode. A mature, ready, and waiting female occupying a decent anemone would not remain lonely. Nemo, if he ever did escape and make it back home, would find the anemone filled with other male clownfish. He would have to wait his turn to meet (and mate with) his father-turned-mother, delaying the happy reunion of son-as-lover with mother-who-was-father.

Though lacking the sharks, jellyfish forest, and surfing sea turtles, when it comes to personal growth and triumph sagas, the real Nemo story offers a far more colorful tale that hinges on the ability of a clownfish to change sex during its lifetime. It’s a strategy deployed by many species of fish and invertebrates—species that never have to wonder what shagging is like for the opposite sex . . . they know.

A Brief Sojourn into Sex-Change Strategies

Under the sea, the boundary between male and female is far more fluid than on land. A little midlife sex swapping is part of the natural lifecycle of everyone from Nemo to the shrimp in your shrimp cocktail. In fact, start naming all the sex-changing animals in the sea, and the list looks like a recipe for bouillabaisse: mussels, clams, shrimp, and a whole slew of fish. There are others, too, such as worms and some sea stars (formerly known as starfish), that don’t lend themselves as readily to a chowder but do exhibit some serious flex in their sex.

Though energy intensive, the ability to alter one’s sex is a strategic way to boost babies per reproductive bonk. Here’s why: in some situations, one sex will make more babies when they are bigger (or older) than when smaller. In human terms, a woman’s fertility peaks in her twenties and declines later in life. But the same doesn’t go for a guy. Instead, he can continue to make babies by hooking up with younger women far into his fifties, sixties, and beyond.

Now imagine that younger guys, with their overeager sex drive and lack of experience, weren’t likely to get much action from discerning females who wished to have their babes sired by only the strongest, wisest, best providers. Under these circumstances, if people wanted to maximize the number of children they could produce, and if we could change sex, it would make sense to start life as a female, making babies by reproducing with older men while you are young and fit. Then, as conception and baby carrying success diminished around thirty-five years old, you would switch to being a male, and kick up your offspring output by finding a pretty young thing to mate with. Voila! You’ve just increased your human production potential.

Of course, you also would have to endure the pangs of puberty twice. In reality, human biology is too prudishly rigid to allow for this kind of flexibility with our sex. The same holds for other mammals, including species such as elephant seals, which would certainly benefit from that kind of flexible strategy: all those small males kicked off the beach by the big alphas could instead start off as females and then morph to males when big and ready to do battle. Alas, it is not an option for most vertebrates.

Fish are an exception. Along with many invertebrates, they aren’t nearly so limited. For them, the cost of sex change is a small price to pay in return for some serious reproductive advantage.

Li l’ Males and Big Ol’ Fat Fecund Female Fish: Protandrous Hermaphrodites

To understand why the real Nemo story reads more like Greek legend than it does Pixar, first you need to wrap your head around the fact the bigger a female fish grows, the more eggs she can make. This “bigger equals more eggs” concept is completely foreign to humans. Our females are born with roughly the same number of eggs—about one million. No matter her height, weight, ethnicity, et cetera, a woman has all the eggs she will ever have before she is born—by about twelve weeks in utero. As she ages, the number of eggs she carries goes down. By the time she hits puberty, only about half of her lifetime egg pool remains (most of these never fully develop and are reabsorbed into the body—only about three hundred to five hundred eggs ever fully mature).

This is not the case in fish (and many other marine species, too). For them, eggs are produced over the course of their female lives, and size matters. The bigger a female is, the more eggs she can fit, and as long as she is healthy, the more eggs she can make. For example, a fourteen-inch-long vermillion snapper will make about 150,000 eggs. A twenty-two-inch female of the same species will make 1,700,000 eggs. That’s over ten times more eggs before the fish doubles in size. So big, old, fat, fecund female fish (affectionately known as “BOFFFFs”) can pump out far more eggs than their younger sisters a few notches down the size scale.

There may be other advantages to BOFFFFs besides sheer increases in number too. Older (and wiser?) females may release eggs over a longer spawning period and more diverse spawning habitats than younger females. This helps them hedge their bets in terms of hitting favorable conditions for larval survival. These factors indicate that BOFFFFs are disproportionately beneficial and perhaps even critical to long-term survival of populations.

That bigger females can carry more eggs is not a trick specific to sex changers. Any large female fish—whether she was born female and stayed that way or started as a male and transitioned to female—contributes significantly more to future generations than a smaller female. But this feature becomes something sex-changing species can exploit, especially for those species that engage in the abnormal behavior of pairing up one-on-one for the season. Such is the case with clownfish, male-to-female sex changers that join seahorses in the minority club of species forming monogamous couples.

As a candy-colored bite-sized fish on a predator-filled reef, clownfish (also known as anemonefish) tend to stick within the confines and safety of their anemone homes. Distant cousins of jellyfish, anemones have a soft body surrounded by rings of stinging tentacles that present a perfect fortress of protection for clownfish, which hide within their waving tendrils. But a good anemone can be hard to find. If you’re an adult clownfish who decides to go looking for a new home, other clownfish will likely chase you away from their already-occupied abodes. No room at the inn for you. But as a juvenile, you’re pretty innocent and pose no competition to the ruling adults, so unless an anemone is particularly crowded, odds are you can stick around. So, young clownfish use their sense of smell to find their way to a good anemone, and once allowed to join a group, they stay.

Confined to an anemone, these fish are stuck with whoever else lives there. It’s kind of like being forced to date only the girl or boy next door. But although there may be four to six individuals living around one anemone, only the two largest individuals will mate: the one and only female with the largest male. And here’s where being a BOFFFF comes in handy. Generally speaking, even a small male has enough sperm to fertilize all of a female’s eggs. The more eggs the female can make, then, the more offspring the couple can produce. So a bigger female benefits them both. By starting off as a male, an individual that hooks up with a big female can produce lots of offspring when small, and then, when his older, bigger partner dies, he can then grow into the female role, get a new mate, and continue the high-level offspring output. This is what clownfish do, and this is why the real Nemo tale doesn’t look anything like the movie.

The trick to an individual clownfish’s sexual success, though, isn’t sex change as much as preventing other adult clownfish from sneaking sex with their mate. Both the top-ranking male and the female engage in some psychological warfare, bullying the other resident clownfish and stressing them out so much that their sexual development ceases. It’s a delicate art form, really. The female torments the largest male just enough to keep him from growing too big (and risk turning into a competing female) but not too much intimidation, so as to which would suppress his manliness. Whipped as he is by the female, the male then takes out his aggression on the next largest individual, but he goes all the way, intimidating that male into suspended maturation. The intimidated then becomes the intimidator, turning to dominate the next biggest, and so on down the line, ensuring that each individual knows his place in the pecking order and remains in pre-pubescent limbo.

Life may not be easy for young, stunted clownfish, but there are advantages to all that torment. When the female dies, the ranking male can quickly convert to female and reap the reproductive rewards: the next juvenile in line simply rises up, grows a pair, and the new couple gets on with the show. Nobody has to venture outside the green zone of the anemone to find a mate.

Clownfish are not alone in their protandrous lifestyle; many oysters also know sex—in the biblical sense—from both sides of the bed. The most popularly consumed species, including those Bluepoints and Belons, Sweetwaters and Wellfleets, Kumamotos and Pemaquids, in all their wondrous, buttery, salty, smoky, earthy, fruity merroir—all have the potential to morph from male to female. Such a talent is also beneficial when you’re an animal that’s stuck in the muck for life.

Glued together as a living rock wall, oyster reefs or “beds” are made up of generations of individual oysters that, as tiny free-swimming larvae, sink down from the surface to attach and grow on the backs of their ancestors. During a season of summer lovin’, oysters contract the two halves of their shelled house, forcefully ejecting enormous numbers of sperm or eggs into the water, where they mix with the gametes of other neighboring oysters. As we will discuss in a few chapters, animals such as oysters that can’t move instead set their gametes free in the open blue to find their complement and fuse. To help increase the odds that fertilization will occur, these animals pump out spectacular numbers of eggs and sperm. Bigger females are advantageous because they can significantly up their egg output—just like BOFFFFs. An adult female oyster may release over a million eggs in one go, and they often have multiple spawning events in a year. Smaller males, with fewer energy reserves, can still make lots of cheap sperm, but it is difficult to make lots of fat-rich eggs and still have energy left over to grow. So, protandry makes sense, with bigger oysters able to divert more energy to female reproduction, which helps everyone.

While size does matter, it is not the only factor controlling sex change. Social cues are also important. As Dr. Juliana Harding, an oyster expert at Coastal Carolina University, notes, “What’s the point of spawning as a male if everyone around you is a male?” Or equally important: why bother changing sex if your neighbor already has? Harding explains that oysters use chemical cues to determine who else is around and of what sex in order to calculate when and if sex change makes sense. “Both size and social cues influence the end product.”

Actual sex change happens after spawning, when the overflowing gonads are finally spent. But in contrast to many sex changers that can make the leap from male to female (or vice versa) in a manner of days, oysters take a bit more time in swapping sex. Harding explains: “It is like phasing out one set of equipment and bringing a new set on line and testing it before getting rid of the old. From an evolutionary standpoint, you always want to be able to spawn as something so as to not miss opportunities to contribute to future generations.” This is also why oysters “trickle spawn,” releasing some eggs or sperm over an extended time frame.

Not all individual oysters change sex, though. In some species, oysters born male stay male while others born male will transition to female after a few years. The difference in the two paths seems to be mostly genetic, with some environmental influence. In the Pacific oyster, for example, it is likely that males born with a genotype MF are true males (similar to male human XY genotype); those oysters with an FF combination (similar to female human XX genotype), however, are protandrous—born male, they may sex-change into female after one or two years. There isn’t a hard deadline for when sex change occurs. Instead both age and the environment can influence the timing: if food supplies are low, or the conditions otherwise harsh, an individual may delay the switch. On the other hand, disease or fishing pressure that targets older and larger individuals may trigger an earlier transition to female—to ensure they pump out a few rounds of eggs before being knocked off. This kind of variable sex change is one example of how external forces can fundamentally affect the sex lives of a species.

The male-to-female transformation is but the tip of the sex-change iceberg, however. The far more dominant strategy (at least in marine fish) for boosting sexual success via sex swapping is the female-to-male route— that’s the pathway of choice for species where big males can effectively rule the school.

This excerpt has been reprinted with permission from Sex in the Sea by Marah J. Hardt, published by St. Martin’s Press, 2016.

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