Dr. Tatiana's Sex Advice to All Creation (19 page)

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But mangrove fish are not most of us. Outbreeding depression could well be an important force for organisms—like yourself—
that have a history of selfing. Thus, we must at least consider whether your offspring will suffer outbreeding depression if you depart from tradition and mate with a male. I can't give you a definite answer, but what we know so far suggests that you can go ahead and whoop it up with your new friend if you want to. Here's the evidence.
Rivulus marmoratus
is found in mangrove swamps up and down the Atlantic coast of tropical America. Males are vanishingly rare: in most populations, they occur only sporadically. In Honduras, however, males make up around 2 percent of the population, while in Belize they are for some reason quite common (around 25 percent). In both places, hermaphrodites regularly allow themselves to be seduced by males. Although the fertility of the resulting offspring has not been measured, outcrossing has no obviously harmful effects. Outcrossed fish are the same size and shape as inbred fish and have no detectable oddities or deformities. So if you're bored with yourself—say yes to sex!
To sum up, incest is not the prerogative of kings, pharaohs, and chieftains; more often, it better befits the humble residents of the king's eyelash follicle than his majesty himself. But whether your blood is regal blue or common red, I advise you not to frolic with family if you carry harmful recessive genes. For the time being, alas, there's no way to know in advance whether you have such genes. I therefore provide some rules of thumb.
 
 
THE PLEBEIAN'S GUIDE TO INCEST
 
1. If you feel a strong aversion to erotic activities with your relations or if you're a hermaphrodite and you possess features
that make selfing difficult, it's probably a sign that incest is not for you. But even when carrying recessive genes, hermaphrodites should still be prepared to self—if possible—in emergencies.
2. If you are not a hermaphrodite, incest is best if you come from a species where males have only one set of genes. If you're not a member of such a species, I urge you to avoid sex with your nearest and dearest. As a last resort, you can kiss your cousins—but stay away from siblings, parents, and grandparents.
3. Finally, if you decide to make a career of incest, make sure to slash your investment in males to a minimum. There's no point wasting energy making armies of big, strong sons if these fellows will just mate with their sisters or their mothers and then die. That's right: the best mama's boys are small and weedy.
EVE'S TESTICLE
H
ow did males and females evolve? What was there before? Why do most species have only two sexes? When is it wise to be male and female both at once? When should you change sex? And what makes a boy a boy and, of course, a girl a girl? It's gender studies—but not as you know it.
Dear Dr. Tatiana,
 
I'm a slime mold—Physarum polycephalum is the name—and
I don't see how I'm ever going to marry and have children. I can only ooze along, so finding partners is difficult. I haven't met one yet. Worse, whereas every other species I've ever heard of has two sexes, my species has thirteen, and I gather that before you can make babies you have to convene them all. I don't see how this is possible, and I'm worried I'm going to end up a dreary old mold. Why are slime molds so oversexed?
 
Looking for a Baker's Dozen in the Forests of Romania
Thirteen sexes? My poor dear, you are seriously deluded: your species has more than five hundred! But don't panic—you don't need to convene them all. Frankly, I think you need a quick lesson in slime mold facts of life.
First things first: what exactly is a slime mold? Most people, if they stumbled across you on a rotting log, would think you were a type of streaky yellow fungus. But nothing could be farther from the truth. Slime molds are a world unto themselves, only distantly related to animals, vegetables, or fungi. There are a couple of different types; you happen to be what's known as a true slime mold. A mature true slime mold is one enormous cell—eas—ily visible to the naked human eye. However, whereas a regular cell is made up of one nucleus surrounded by a dollop of cytoplasm, the cell of a mature slime mold is a big mass of cytoplasm filled with millions of nuclei. This entity creeps along, devouring any microbes in its path. It does not copulate—and hence has no need to find a partner. Instead, when the time comes to have sex, it grows into a stalked fruiting body that looks like a tiny blistered lollipop. This structure releases spores into the air just as a flower might release pollen, and the spores develop into sex cells.
What's a sex cell? There's no mystery about that. A sex cell carries one complete set of your genes. Its mission is threefold: to find, recognize, and fuse with a suitable sex cell from the same species. What do I mean by “suitable”? I mean a sex cell of a different sex.
You see, sexes simply define who can reproduce with whom. Or, to be more precise, sexes define which sex cells can fuse with each other. Among animals, then, there are two types of sex cells, big (eggs) and small (sperm). A female or a male makes only one type; a hermaphrodite makes both. It's a truism that two sperm cannot fuse to form an embryo, and neither can two eggs. The only possible combination is one egg and one sperm.
Among slime molds, however, the situation is different. Along with organisms such as green algae, seaweeds, diatoms—tiny golden algae that secrete beautiful, symmetrical shells—and many of nature's more obscure creations, slime molds make sex cells that are only one size, a condition known as isogamy. When size is irrelevant, other features of a sex cell determine its sex. In principle, these could be anything—the simple presence or absence of a particular chemical on the surface of a cell would be one possibility. In your case, alas, it's nothing that straightforward.
Slime mold sexes are determined by three genes, known as
matA, matB,
and
matC.
Each of these genes comes in several variants—
matA
and
matB
each have thirteen known variants (which is presumably where you got the erroneous idea you have thirteen sexes), while
matC
has three. Now, bear in mind: as a mature slime mold, you have two copies of every gene. So let's suppose you have variants 1 and 3 of
matA,
variants 2 and 4 of
matB,
and variants 1 and 3 of
matC.
When you turn into the blistered lollipop and make your sex cells, each of them receives one complete set of genes—including one each of
matA, matB,
and
matC.
Each sex cell could thus receive any combination of the variants of these genes: one sex cell might have
matA1, matB2, matC1;
another might have
matA3, matB2, matC1—
you get the idea. As an individual slime mold, you are therefore capable of producing sex cells of eight different types—all combinations of your
As, Bs,
and
Cs.
If you want to impress people, just call yourself an octosex. Out there in the forest, of course, other slime molds have different combinations of the variants of these genes; when you count up all possible combinations of
matA1—13, matB1—13,
and
matC1—3,
you get more than five hundred. (And indeed, since more variants of these genes probably await discovery, the slime mold sexes tally may go even higher.)
When your sex cells go forth into the world—and slime mold
sex cells are unusually independent; they are even able to eat (imagine a sperm stopping to have a snack)—their mission, as I've said, is to find a suitable partner to fuse with. And in your case suitable means that your partner has different variants of each of the three genes. So a
matA1, matB2, matC1
sex cell could fuse with a sex cell carrying
matA12, matB13, matC3,
but not with one carrying
matA12, matB2, matC3.
Complicated, eh?
All the same, your system is not freakish. On the contrary. Theories predict that isogamous organisms should have an embarrassment of sexes and that the really outlandish thing is to have only two. Let me walk you through the reasons why. Imagine the world from a sex cell's point of view. And imagine that you're in a population that has zero sexes—every sex cell can fuse with every other. In such a population, finding a mate is as easy as it gets. There is a drawback, however. Zero sexes cannot prevent inbreeding. If you encounter a sex cell from the same parent, you can go ahead and fuse with it.
Now imagine that you're in a population that has a large number of sexes. The larger the number of sexes, the easier it is to find a suitable partner to fuse with. At the same time, you become less likely to commit incest: sex cells from the same parent are much less likely to be allowed to fuse with each other. (In the slime mold case, a sex cell of a given type can fuse with only one-eighth of the other sex cells produced by the same parent.) In other words, a large number of sexes simultaneously increases the probability of finding a mate while reducing the risk of inbreeding.
How do you get from zero sexes to hundreds? Taking the first step—from zero to two—may be quite difficult, and exactly how it can happen is controversial. (Obviously the transition cannot be all that difficult, though, since we know it has happened
repeatedly.) Be that as it may, once this initial hurdle is leapt, evolving more than two sexes is a snap. The reason is that if an individual starts making sex cells of a third sex, these will be able to fuse with sex cells of both the other sexes (but of course not with itself). At first, this new sex has an advantage because it can fuse with a larger proportion of the population than the other sexes can. The genes for the new sex will spread—until the population reaches an equilibrium where all three sexes are present in equal frequencies. If a fourth sex should then appear, the same thing would happen. Because being a new sex is always advantageous, the number of sexes will gradually drift upward.
And yet, as you correctly observed, most other isogamous organisms do have only two sexes—the least convenient situation with respect to finding a mate. Or, to put it another way, evolving more than two sexes is easy and has an obvious advantage; yet most isogamous organisms are stuck at two (though not male and female). Which suggests that there is some other power at work, something that strongly constrains the number of sexes that isogamous organisms can have. But what could it be? And how come slime molds are exempt?
No one knows for sure what the constraining factor is. The most likely candidate, however, is the need to control the inheritance of unruly genetic elements in the cytoplasm. You see, in addition to the regular genes of the nucleus, most organisms harbor other genetic elements: mitochondria, for example, or chloroplasts. (Chloroplasts are found within the cells of plants and green algae and are responsible for manufacturing energy from sunbeams; mitochondria are found within almost all cells, except those of bacteria, and metabolize carbon compounds.) These elements reside in the cytoplasm of the cell, often in extremely large numbers. They are thought to be the remnants
of bacteria that once, long ago, were independent organisms. At some point in the ancient past, the bacteria took up with primitive cells, trading energy for shelter, and as time went by, they became unable to function on their own. Now, they have just a few genes left to them, a rump genome. But, as everyone knows, rumps can be troublesome.
Problems are most likely to arise if mitochondria and chloroplasts are inherited from both parents. Then, the mitochondria (say) of the parents may compete with each other in ways that harm the organism. For example, mitochondria from one parent could attempt to exclude mitochondria from the other parent from the sex cells; such goings-on may result in the mitochondria being less efficient at what they're meant to be doing—metabolism. The easiest way to prevent any problems of this sort is to make sure that mitochondria—and chloroplasts, if you've got them—are inherited from only one parent.
Why would this constrain the number of sexes to two? Well, the idea is that strict control over the inheritance of these elements is overwhelmingly important, and by far the simplest method of control is to have one sex that never gives them and one sex that always does. A number of isogamous organisms have mechanisms to ensure that only one parent will pass on these elements. The green alga
Chlamydomonas reinhardtii,
for example, has sex cells of two types, known as plus and minus. The plus type transmits chloroplasts, the minus type mitochondria.
There's another piece of circumstantial evidence that controlling these elements constrains the number of sexes. Two groups of organisms—mushrooms and single-celled critters called ciliates—have sex not by making sex cells but by two individuals swapping half a nucleus. (This system has the odd effect of making you become genetically identical to a total stranger—the two of you are suddenly identical twins.) Crucially, no cytoplasm
changes hands, and these organisms have no need to regulate the inheritance of mitochondria. Sure enough, in these groups the number of sexes can be opulent.
Schizophyllum commune,
a pinkish, hairy mushroom that grows on tree trunks, has as many as twenty thousand different sexes.
So you see, what really makes slime molds exceptional is not so much the number of sexes but the fact that you have lots of sexes
and
you merge the cytoplasm from two parents. How do you get away with it? Are your mitochondria better behaved than those of other species? Nope. The key is that your mitochondria are still inherited from only one parent. The gene
matA
supervises the elimination of mitochondria from one parent or the other. There's a hierarchy of the variants so that if cells carrying
matA12
and
matA2
fuse, the mitochondria that came with
matA12
will be destroyed, whereas if
matA12
and
matA1
fuse, the mitochondria accompanying
matA1
will get the ax. I imagine that this system doesn't evolve often because it is difficult to get it to work—and I salute slime molds everywhere for making it a success!
Dear Dr. Tatiana,
 
In the whole of my species, the green alga Chlamydomonas moewusii, I think I'm the only male: I make small, elegant sex cells, everyone else makes big, clumsy ones. But being the only male is no bed of roses. The big, clumsy sex cells can fuse with each other, so I'm not especially in demand; in fact, I suspect that my sex cells are being discriminated against. It's just not fair. What's going on?
 
Ready to Litigate in Tallahassee
I suspect you're just a man whose time hasn't come. Rather than being the first father of a great tribe of green algae, you'll probably die without begetting anybody. Why? Well, your species is isogamous—and you are just a mutant who produces smaller sex cells than everyone else. When a sex cell of yours fuses with a regular sex cell, the resulting cell, known as a zygote, will be smaller than usual. This will almost certainly reduce its chances of survival.
You've been unlucky. Species containing males and females have evolved from isogamous species over and over again. Indeed, although isogamy has long gone out of fashion for plants and animals, the distant ancestors of both groups are thought to have been isogamous. So what's the secret of making the transition from being an isogamous species with two sexes to having males and females? Let me say at once that there are lots of ideas—but no definitive answers.
The essential problem in the evolution of males and females is to imagine forces that favor individuals who make either big sex cells or small sex cells but not sex cells of intermediate size. At first glance, it's easy to imagine how an individual could benefit from making small sex cells—small sex cells can be produced in large quantities, and an individual who makes more sex cells than his rivals increases the number of other sex cells he can potentially fuse with. The problem is, though, as you've found, producing lots of small sex cells won't get you anywhere if these small cells ruin the zygote's chances of survival. Indeed, if we make the reasonable assumption that for a zygote to be viable it must be at least as large as the zygote that results from the fusion of two isogamous sex cells, then males and females can only evolve if, at the same time that some individuals are starting to make smaller cells, other individuals are starting to make bigger ones.

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