Dr. Tatiana's Sex Advice to All Creation (18 page)

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Authors: Olivia Judson

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After settling in and perhaps taking a light supper of—I'm afraid—your blood, she started to lay her eggs, about eighty in all. A couple of days later, the eggs hatched, the little larval mites wriggling backward out of their eggshells. First to emerge were the males of the brood; then came all their sisters. The males grew up faster than their sisters, prepared one of the innermost galleries of your ear as a bedchamber, carried their sister-brides thence, and even helped them out of their old skins as they finished their final molts into adulthood.
You needn't feel self-conscious about having your ear infested by mites—such things happen in nature all the time. Army ants—the ones that sweep through rain forests killing everything in their path—have one species of mite that lives on their antennae and another that lives on their feet. Hummingbirds get mites in their nostrils when they drink at flowers. The mites don't cause the birds to lose their sense of smell, since they are just hitching a lift between flowers. But they are still a nuisance: nectar thieves, they can slurp up as much as half of the nectar a flower produces.
Humans play host to the (mostly harmless) mite
Demodex folliculorum,
which lives in eyelash follicles, as well as to
Demodex brevis,
which occupies the sebaceous glands. Fruit bats have mites on their eyeballs. Birds have mites inside the quills of their flight feathers.
But coming back to the orgy in your ear, there is one thing I'd like to draw your attention to. Namely, that the orgy embodies what some would consider paradise. Of the eighty or so eggs laid by the mother mite, one or perhaps two will have hatched out males; the rest will have hatched out females.
This deserves notice because, in general, dramatic deviations from a sex ratio of one to one are rare. Males and females of most species are born in roughly equal numbers. The reason for this balance was first explained by Ronald Fisher—the same fellow who suggested females might mate with attractive males in order to have sexy sons. In essence, his argument is one of supply and demand. Suppose girls were more common than boys. Then, any parent with a predisposition to have sons would have more grandchildren than a parent with a predisposition to have daughters because boys would be scarcer and more likely to find mates. The gene for sons would spread—and as it did, the sex ratio would become less skewed. Since the same argument applies if the initial skew were toward more boys, the only stable situation is a sex ratio of one to one, and any deviation should thus be quickly and automatically corrected.
Humans may provide an instance of such a correction. During wars, large numbers of men are killed, skewing the sex ratio toward women. Therefore, one might imagine that a sex-ratio adjustment would occur in response to wars. Consistent with this, a significantly larger proportion of boys were born in the immediate aftermath of each world war than before the outbreak
of hostilities. (I should stress that the mechanism for this is unknown and the finding may be a coincidence rather than a demonstration of Fisher's principle in action. But it is provocative nonetheless.)
A pronounced departure from a one-to-one sex ratio, therefore, indicates that something unusual is afoot. The “something” can be sinister: numerous parasites meddle with their host's sex ratio in order to increase their own transmission. In the common woodlouse, for instance, microbes transmitted only through eggs act to convert genetic males into females. The wood lemming—a tiny, stocky rodent with a furry tail that lives in the bogs and forests of northern Europe, Siberia, and Mongolia—has a maverick chromosome that skews the sex ratio toward girls. As a result, the typical wood lemming population is more than 70 percent female.
More benignly, a highly skewed sex ratio is one of the trademarks of close incest. In
Syringophiloidus minor,
the mite that lives in the quills of the house sparrow, each female lays twelve eggs, only one of which will hatch into a male. Likewise,
Acarophenax mahunkai,
our aghast correspondent from Arkansas, would most likely have had his fifty sisters to himself. In short, among the unrepentantly incestuous, males are produced with extreme thrift.
The reason for this was discovered by Bill Hamilton, one of the most original and important evolutionary biologists of the twentieth century. He pointed out that among inbreeders a female will often arrive at a new home—be it a coffee bean or a date stone, your ear or my eyelash follicle—that no one else may ever attempt to colonize. Under these circumstances, the argument for a one-to-one sex ratio breaks down. When a female is isolated, her reproductive success depends only on how many daughters she has: she will not gain any additional grandchildren
from her son's seducing the daughters of other females, because there are no such individuals to be seduced. Therefore, the original matriarch should produce just enough sons to inseminate her own daughters: any more would be a waste of time and energy.
In general, then, habitual incest allows for all kinds of savings with respect to the structures involved in male function. For hermaphrodites, it means a minimal investment in male apparatus. For example, in the hermaphroditic mussel
Utterbackia imbecillis,
a parasite that lives on the gills of freshwater fishes, the proportion of its body devoted to sperm production diminishes as incest—in this case, selfing—increases. Selfing plants dispense with showy flowers: they have no need for extravagant displays to attract pollinators. Similarly, incestuous females do not gain by creating huge, macho sons—all that matters is that the boys live long enough to shag their sisters. Sure enough, the sons of inbreeders tend to be precocious runty fellows with short life expectancies. Often, they do not feed during their brief glimpse of life on earth; many don't even have mouths. Soon after their ecstatic orgies are done, these males die, usually without having left their natal bean, or quill, or ear. I'm afraid, dear moth, that once your tenants have disembarked onto scented blossoms to wait for the passing of a fresh host, their brothers' rotting bodies will remain, a leperous ghost colony in the inner porches of your damaged ear.
You do have something to thank them for, though. The first mite apparently leaves some sort of trail, for if a second or a third mite should get on board to start a family, the new arrival will go to the ear that's already occupied. Indeed, if your deaf ear is already overflowing with occupants, the mites of this species will not invade your intact ear—just as the old rhyme says. They would rather get off again and wait for a new moth than deafen
you to the ultrasound squeaks of bats. This makes sense: if you die, they die. But their having evolved such an unerring response suggests that multiple boardings are not uncommon. And that, in turn, suggests that incest is not always the only choice.
If other females begin to show up in your ear, sons have a chance to mate with females who are not their sisters—and the advantage of producing more males starts to increase. Thus, the more females who colonize a particular spot, the more sons each one should produce and the more balanced the sex ratio should become. Take
Nasonia vitripennis
, a tiny wasp that lays her eggs in blowfly pupae. When the female finds a pupa, she drills through the wall and injects a venom that kills and preserves the developing blowfly. She lays eggs, of which perhaps 10 percent will be males, and then heads off to seek new pupae. If, however, she arrives at a pupa that is already occupied, she will adjust her brood so that she has more sons.
How does she do this? Well,
Nasonia vitripennis
is one of those species where males hatch from unfertilized eggs. This system readily allows an exact control of the sex ratio: each mother can determine how many sons and daughters she will have by how many eggs she fertilizes. The mites inside your ear, however, have the other genetic system that aids and abets incest, the one where males develop from fertilized eggs but the father's genes are promptly discarded from male embryos. At first glance, it seems unlikely that females in this system would have the ability to fine-tune the sex ratio of their offspring according to circumstance. And yet—amazingly—they seem to be able to. Experiments on
Typhlodromus occidentalis,
a mite that has paternal genome elimination, show that females produce more sons in the presence of other females. Does such a shift also occur in your ear? No one knows, but I would guess it does.
Dear Dr. Tatiana,
 
Like any decent, upstanding mangrove fish—that's Rivulus marmoratus to you—I've always fertilized my own eggs. But this evening I came home to the burrow I share with a friendly great land crab and I found a stranger had moved in. He claims that he's a mangrove fish as well—but that he's a real man, not a bit of both like me. He says he wants us to do all sorts of terrible things together. It sounds like fun. But will it do me any harm?
 
Gagging for It in Florida
Normally, I'd say go for it. But in your case, we need to consider the situation carefully. You mangrove fish have some bizarre customs, one of which is your habit of clambering out of the water to spend time on land, locomoting with flips, wriggles, and jumps. This explains how you get into the burrows of the great land crab—the entrance to a crab's home is usually reachable only from terra firma. Even more remarkable, you can survive more than two months out of water—quite a feat for a fish.
To a geneticist, however, what makes you unusual is the fact that you're the only vertebrate—the only animal with a backbone—known to self-fertilize. Indeed, hermaphrodite mangrove fish are incapable of spawning with one another; they can only spawn with individuals who are pure male. When males are rare, as they are in Florida, a population of mangrove fish consists of hermaphrodites who have been selfing for generations.
With that in mind, let's examine the risk you could run if you mate with a male. You've heard of inbreeding depression? Well, ironically enough, there's also something called “outbreeding depression.” The idea is that sometimes unions between distantly related individuals produce offspring who have a poor chance of
surviving or reproducing—a worse chance, in fact, than the offspring of more closely related parents.
In principle, outbreeding depression can occur for two reasons. First, the partners may have genes that cannot act effectively in concert. The most obvious, most prevalent, and least interesting example of this comes about when an organism tries to mate with a member of a different species. Such bestial couplings are generally infertile; after all, species are defined as groups that cannot interbreed. But when species have recently separated, offspring may still result from cross-species fornications. The coupling of a mare and a jackass famously yields a mule—but note that outbreeding depression still strikes, since the mule is sterile.
Less extreme outbreeding depression may indicate that populations are in the process of diverging into separate species. In pink salmon, for instance, individuals have a fixed two-year life cycle. Thus, a given river may have two salmon populations separated in time: even-year salmon and odd-year salmon. Under ordinary circumstances, ne'er the twain shall meet. When they do meet—as eggs and sperm in the test tubes of a laboratory—they beget offspring that are viable but that don't survive as well as purebreds.
The second potential cause of outbreeding depression is the external environment. Suppose individuals have evolved features that help them cope with particular local conditions. Then, mating with an individual from somewhere else, who is therefore not well suited to prevailing conditions, may break up favorable gene combinations. Consider the soapberry bug. This creature makes a nuisance of itself by feeding on seeds of the soapberry tree. To get at the seeds, it pierces the fruits with its beakish mouthparts—which are the perfect length for reaching the seeds. Recently, however, the soapberry bug has started feeding on seeds of the
round-podded golden rain tree. In this plant, the seeds are buried more deeply within the fruit—and the ideal beak for a soapberry bug needs to be much longer. As a result, soapberry bugs have evolved to specialize on one tree or the other: short-beaked soapberry bugs live on soapberry trees, and long-beaked soapberry bugs live on round-podded golden rain trees. Sex between members of the two populations could disrupt beak length, which could make it impossible for the progeny of such crosses to feed.
Before you conclude that you're damned if you inbreed and damned if you outbreed, I should say that documented cases of outbreeding depression within a species are far fewer than documented cases of inbreeding depression. True, outbreeding depression has been studied less. But that's not the only reason for the difference. In many species, inbreeding depression drives the evolution of elaborate mechanisms that stop organisms from mating with their relations. In contrast, mechanisms to avoid outbreeding are virtually unknown. Thus, to the extent that it occurs, outbreeding depression is probably not a cause of mating patterns but a consequence—and a trivial one, at that. Let me give you an example. Outbreeding depression is most likely when two mates come from populations that don't normally interact. After all, pink salmon from different cycles don't mate, because they don't meet. In the case of some plants, outbreeding depression may arise as a consequence of the activities of pollinators. Bees often fly fixed distances between flowers—and it's not uncommon for crosses between plants more than one bee flight away to show outbreeding depression. Therefore, my guess is that for most of us outbreeding depression will turn out to be of little concern.

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