The Wilder Side of Sex
by John Tidwell
So there you are, gazing proudly at all those cute,
colorful reef fish in your saltwater aquarium, serene
in the knowledge that you know precisely which fish
is what, right down to the species’ names and
the individuals’ genders. But wait—weren't
there supposed to be two red female stoplight parrotfish?
How the heck did a green male get in there?
Better get used to it—he used to be a she. In
the wild, gender ambiguity is natural and practically
anything goes, as long as it works. For the past couple
billion years, plant and animal species have tried all
sorts of ways to solve the problem of how to survive
and make as many babies as possible. In that time, they
evolved a mind-reeling array of solutions.
From protozoa to pill bugs to porgies, changing from
one sex to another is not just biological ingenuity,
it’s a way of life. It’s also shocking proof
that gender is a much more versatile, flexible tool
in Mother Nature’s kit than anyone had previously
realized—and is kinkier than you ever imagined.
Your very green, very male stoplight parrotfish eyes
you knowingly through the glass, as if to say “You
ain’t seen nothin’ yet!” What in the
name of Charles Darwin is going on here?
The Spice of Life
Consider the humble two-banded anemonefish (Amphiprion
bicinctus) nestled like a sultan upon a bed of
pink-tipped sea anemone tentacles. Here in the shallows
of the Red Sea, this small, orange-and-white fish lives
in cozy symbiosis with its flower-like protector, rarely
ever venturing farther than a tentacle’s reach
from home. When our male anemonefish chances upon another
male of the species, what happens? Does he puff himself
up, large and frightening, challenging the interloper
to a battle royale? Not at all. Mr. Amphiprion starts
to transform into a Ms. and invites the other fish to
mate. Nobody gets hurt and in time both get to loft
their genes into the next generation. Perched upon their
anemone, the two will live in prim monogamy until death
do them part. At which time, the survivor may once again
shift gender to secure a mate.
Consider the lilies-of-the-valley (Convallaria
majalis) in a glade as they nod their tiny white
flowers in the afternoon sun. Look a little more closely,
and you might notice that those pristine flowers have
male and female sex organs simultaneously. These lilies,
like a wide variety of flowering plants, are hermaphrodites:
They have sex with, and fertilize, themselves.
Beneath the lilies lies a rotting log, home to a tiny
organism that isn’t a plant or an animal or a
fungus. It looks like a blob of scrambled eggs, but
in fact it’s a slime mold (genus Physarum),
an otherworldly creature with 29 variants of sex-controlling
genes, dispersed among eight different types of sex
cells. To ensure genetic diversity, each slime mold
sex cell can only fuse with a sex cell that has completely
different variants of genes than its own. If you calculate
all the possible combinations of genes and sex cells,
you will find that Physarum have more than
500 different sexes. Reproduction for slime molds may
be complicated, but it’s never boring.
Weird sex is all around us, in the earth beneath our
feet, the air above our heads, and the sea from which
we all evolved. In fact, sex itself remains an unanswered
biological enigma that has confounded scientists for
decades. Since the 1960s, when traditional models of
sex were scrapped (due to lack of evidence), evolutionary
biologists have spawned great schools of competing theories
to explain why sex exists at all. But in this Darwinian
scramble, one theory—The Red Queen—has emerged
in recent years to dominate them all.
The Red Queen
This poetic model, plucked from the pages of Lewis Carroll’s
Through the Looking-Glass, envisions a frenetic
world where the notion “every gene for itself”
reigns supreme. Just like Alice and the Red Queen, who
find themselves running to stand still, evolution is
a treadmill where all creatures must run like mad just
to stay in the same evolutionary spot.
In his 1993 book The Red Queen, science writer
Matt Ridley explains that in this theory, baby-making
is more business than pleasure. “Sex is not about
reproduction,” he writes. “Gender is not
about males and females, courtship is not about persuasion,
fashion is not about beauty and love is not about affection.”
It is about getting your genes into the next generation,
and trumping the Terrible Three: predators, parasites,
and the neighbors. Of that trio, parasites rank as the
greatest foe. According to Ridley, parasites have been
more deadly to our species (for example) than all the
lions, wars, and accidents that have ever killed anyone.
World War I killed 25 million people in four years,
he writes, while the 1918 flu that followed killed 25
million people in four months.
Sexual reproduction helps individuals get ahead in
this great struggle, allowing creatures to mix their
genes and produce hybrid offspring that might have better
resistance to parasites. Asexual creatures, which are
nearly always female, can make more babies than their
sexual neighbors, but they are all clones—nearly
exact copies of their mothers.
If an asexual mother were vulnerable to say, pneumonia,
so would all her daughters be, and an entire generation
could be wiped out by a sneeze. Many evolutionary biologists
surmise that the reason males exist at all, and therefore
sex exists, is to provide an extra genetic edge, even
though it means that only half of a population can actually
But just because some creature wriggling in the muck
billions of years ago invented boys and girls doesn’t
mean parasites are beaten. The credo of the Red Queen
is that for every action there is a reaction: Each time
you mount a defense, the bugs will come up with a way
around it. Even sex itself isn’t the only way
to stay healthy and cover the Earth with progeny. For
lots of creatures sexual reproduction is a choice, one
wrench in their biological toolbox.
Boys Will Be Girls and Girls Will Be Boys
Water fleas (genus Daphnia) are freshwater
crustaceans that look like tiny translucent Pokemons,
hopping through the water on fan-like fins that never
seem to tire. When tasty algae are plentiful and there’s
lots of elbow room, everyone is female and asexual.
But if the living gets too easy, and the pond becomes
overcrowded with Daphnia, suddenly males are
hatched. They mate with females, which produce eggs
that hatch when the pond gets flooded again with rain.
For these water fleas, sex can be turned on or off as
needed. Daphnia aren’t the only ones
to do this either: Your lovely green lawn remains asexual
until you forget to mow it. Then sexual flower heads
emerge and send pollen and seeds off on the wind. Kinky?
Perhaps, but it also indicates that the world around
us plays as powerful a role as DNA in determining how
There are more ways for gender to be decided than the
genetic X meets Y that mammals and birds seem to prefer.
Other beasties depend on cues from their surroundings.
Some reptiles, such as alligators (genus Alligator)
and painted turtles (genus Chrysemys), let
the sand their eggs are buried in make the choice: Hot
sand makes males, and cooler sand makes females. Some
microscopic parasites have also been found to commandeer
the sex lives of arthropods (insects, crustaceans, and
spidery types), and determine not only the gender of
their hosts’ offspring, but also the very direction
of their evolution (see sidebar).
“These days you can’t even talk about genes
being separate from the environment, the lines are so
blurred,” explains Marlene Zuk, an evolutionary
biologist from the University of California, Riverside.
“Whether it’s reproduction or even gender
determination, you start realizing that you can’t
separate out the purely genetic because how the genes
are manifested depends on environmental forces.”
That’s Environment with a big E, which means
not only the Terrible Three, but also weather, geography,
the local social group, and other organisms’ genes
that are busy attacking your own (which is what happens
when you get sick). What does all this have to do with
sex change? Everything. For now, let’s stick with
animals. Any critter that bends its own gender is, by
definition, a hermaphrodite, with sex cells or organs
of both male and female. Hermaphrodites come in two
basic flavors: Those that permanently function as both
genders are known as simultaneous hermaphrodites, while
those that shift back and forth are called sequential
hermaphrodites. One of the best places to find either
of these varieties, should you be inclined, is beneath
the ocean waves.
Here at the local reef, having the ability to fertilize
yourself is great if you’re immobile, like barnacles
or coral polyps: You don’t need to depend on whatever
mate happens to slither by. For spineless creatures
on the go, being double-sexed often leads to orgies.
Sea hares (Aplysia dactylomela) are snails
without shells that are male in front and female behind,
leading them to form erotic daisy chains that can involve
a dozen or more animals at once. Slipper limpets (aptly
named Crepidula fornicata) are male while free-swimming
and female when they settle down on a rock. When a male
swims by a female slipper limpet, he flops onto her
to mate. If another male lands on top of him, the lower
male turns female, and they clasp. And so on, and so
on. Scientists have recorded up to 14 limpets at a time
pancaked into towers of lust. Invertebrates take the
prize for most sexes, genders, sex organs, and acrobatic
means of coitus, but when it comes to vertebrate hermaphrodites,
something is definitely fishy.
Hamlets (genus Hypoplectrus) are small tropical
fish that sometimes are blue, but are certainly not
melancholy. Like most reef fish they are hermaphrodites,
but of the simultaneous persuasion. When two hamlets
meet they don’t soliloquize, they pair and have
a lovely time assuming one sex role and then the other.
And pair they do. Hamlets hold the sex-shifting record,
switching from one set of gonads to the other and back
in 30 seconds or less, with an average of 14 spawns
in one day. An amphibious Caribbean killifish called
Rivulus marmoratus takes this even further:
It doesn’t even look for a mate, but fertilizes
itself. Rivulus is the only vertebrate known to science
that can do this. But such creatures are an anomaly,
a rare few species that are acrobatic and have the energy,
will, and ability to haul around two separate reproductive
tracts (not an easy proposition, evolutionarily speaking).
Wouldn’t it be easier to start as one gender,
and then carry the other in your wallet, just in case?
Welcome to the world of the sequential hermaphrodites.
Why Can’t A Woman Be More
Like A Man?
Pity the poor female cleaner wrasse (Labroides dimidiatus)
who has lived happily in a harem with her sisters, protected
and serviced by a virile, iridescent male. One day,
tragedy strikes and Mr. Wrasse vanishes. Maybe he was
eaten, or scooped up for somebody’s aquarium.
Who knows—he’s gone. What’s a girl
to do? Be the man, of course.
Ross Robertson of the Smithsonian Tropical Research
Institute in Panama has been studying sex-changing reef
fish for decades. In his research on polygamous wrasses,
Robertson has seen it all happen again and again: As
soon as the male is gone, the largest female in the
harem begins to behave like a male: chasing the girls,
swaggering around, and being macho. Inside her ovary,
often within 24 hours, says Robertson, the female’s
immune system is reabsorbing her eggs and turning on
the testosterone. Within a week she (or rather he) will
be producing viable, healthy sperm.
But how’s it done? The trick, says Robertson,
is that these fish may be born female, but in a tiny
pocket in their ovaries are hidden little stashes of
undeveloped sperm cells, waiting for their moment to
shine. When the social environment demands it, girls
become boys. And that’s the key—sex shifting
only occurs where it’s needed for survival. You
don’t see sex change in open-water fish that school
and breed in large shoals. With clouds of sperm and
eggs swirling around in the crowd, who cares what gender
you are? But when fish are living in a very specific
place, like a sea anemone or a particular head of coral,
in a very socially stratified community, being able
to swing both ways sexually means you will always get
a date (and your eggs fertilized).
And what of our sweet young anemonefish with the hunky
boyfriend and a gaggle of babies? How does such a thing
happen to a guy? Actually in much the same way, says
Robertson. Among these AC/DC hermaphrodites, females
that turn into males are called protogynous, while boys
that become girls are protandrous. Since the default
sex for most vertebrates is female, more creatures tend
to be protogynous. But what gender you are (at that
particular moment) is of less importance among the sex-changing
set than how big you are. “In protogynous fish
it pays to be female when you’re small and male
when you’re large,” says Robertson. “If
you can’t set up your territory when you’re
small because you’ll get the hell kicked out of
you by a bigger male, then you’re better off being
female. Once you get to a certain size, and you have
the capacity to hold territory and get a harem, then
you’re better served being male.”
The flipside for protandrous fish is that it’s
easy for your body to make sperm when you are small,
because sperm takes less energy and resources than eggs.
But when you get big and beefy, you have more stuff
to make large, nutritious eggs, and then it’s
better (reproductively) to be a girl.
Then there are some species that put sex shifting into
overdrive. The small-eyed goby (Gobiodon micropus)
is a protogynous fish that is ready to dance to any
tune. Put her with a larger female, and she becomes
male. Plop down a bigger, meaner male, and this goby
turns back into a female. And contrariwise.
Protandry and protogyny are not just for fish either.
You can find them among the bees of the air and the
sawgrass of the fields. Where you don’t find hermaphrodites
of any stripe is in mammals and birds. How come? Why
aren’t we all sex-changing hermaphrodites? Ross
Robertson has a convincing answer: “In fish, all
you’re doing is changing the contents of a bag—that’s
all a testes or an ovary is in a fish. Whereas in mammals,
you have an enormous number of differences between the
sexes, probably controlled by a whole host of genes.
I mean, replumbing the entire animal, redoing the whole
skeleton, changing its brain and everything else, would
be very difficult and extremely costly for the animal.”
Alas, the truth is no one really knows for sure. Asking
evolutionary biologists such questions is like asking
a group of Englishmen the best way to make tea: You
get a deluge of conflicting and adamant opinions. These
scientists do agree that in nature, gender is not something
fixed and immutable, but a survival strategy. Some use
genes, some use temperature, others use the social club,
and some (probably most) use all of the above. The only
rule is “survive and reproduce.” If you
can manage that and it feels good, do it! “And
that,” says the Red Queen with a smile, “Is
what it’s all about.”
—John Tidwell is a freelance journalist living
in Silver Spring. He has written numerous articles on
conservation for ZooGoer, as well as articles
on history for American Heritage and American
ZooGoer 33(2) 2004. Copyright
2004 Friends of the National Zoo.
All rights reserved.