Dr. Tatiana's Sex Advice to All Creation

by Olivia Judson

  Delusions of divinity play no part, however, in the evolution of close incest among insects, pinworms, and mites. So what accounts for their enthusiastic embrace of it? Crucially, many insects and mites and all pinworms have few recessive genes, which means negligible inbreeding depression. But why do these critters get away with fewer recessive genes than the rest of us? The answer lies in the marvelous genetic systems they employ.

  Two particular genetic systems—each of which has evolved several different times—are extremely efficient at purging recessive genes. The first, known as haplodiploidy, is the more common. In this system, females, like humans, are diploid: they receive two copies of each gene, one from each parent. Males, in contrast, are “haploid”: they hatch from an unfertilized egg and thus receive only one copy of each gene, from their mother. In other words, males have no father and females don’t need to mate to produce sons. That’s right: a boy’s mother may be a virgin.

  This permits all sorts of jolly debauchery. Take the button beetle Coccotrypes dactyliperda. This creature lives in grottoes that it hollows out of date stones (or, indeed, buttons—yes, I do mean the buttons on clothes). Brother and sister button beetles can mate with each other right after hatching—but that’s just the beginning. On arriving at a new home, a female who failed to mate with one of her brothers in the date stone of her birth digs out a grotto and then lays a small clutch of unfertilized eggs. These develop into males. She mates with the first to hatch and then eats him and his brothers before laying a large brood of daughters—and perhaps one or two more sons for her girls to mate with.

  Worse: the wasp, Scleroderma immigrans. The female paralyzes beetle larvae with repeated stings before drinking their blood. Next, she plasters their bodies with eggs so that her growing children can also enjoy the bloody feast. In this species, a mother not only mates with her son but also goes on to mate with a grandson produced by a daughter from the first incestuous liaison. It puts Oedipus in the shade.

  The second genetic system is less versatile, less common, but much more weird. Called paternal genome elimination, it is practiced by various mites and a smattering of insects. Here, males arise from fertilized eggs as they would in humans. But then—this is the weird part—early in the embryo’s development, the cellular machinery inactivates or destroys the father’s genes. The result is that once again, to all intents and purposes, males have only one set of genes.

  So you see, in both systems harmful recessive genes never have a chance to accumulate. Since males have only one copy of each gene, recessive genes are never hidden behind healthy ones: any flaws are immediately apparent and thus exposed at once to the full fury of natural selection. This means that males bearing harmful recessive genes will die. On the other hand, inbreeding depression is unlikely in the event of incest. When your mitey ancestors first turned to their siblings for comfort, recessive genes didn’t stand in their way.

  Dear Dr. Tatiana,

  I’m a true armyworm moth, and I’ve gone deaf in one ear. I’ve read this is from having too much sex. Trouble is, I’m (sob) still a virgin. So what’s happening to me?

  Piqued in Darien

  Be assured, you have nothing to worry about. It’s just that your inner ear is now hosting a torrid, incestuous orgy. Remember the rhyme you learned as a caterpillar?

  A moth who can’t hear

  At all in on ear

  Is probably quite

  A home to a mite

  Dichrocheles infest

  While the moth is at rest

  An unlucky event—

  Mites never pay rent.

  Yet once they’re on board

  They are all in accord

  ’Cause they’ve learned to perfection

  Though natural selection

  (Or heard from an oracle)

  To invade just one auricle.

  For a moth who’s stone-deaf

  To the ultrasound clef

  Is lunch for a bat.

  No lunch for a bat

  What happened is that one evening when you stopped to sip nectar from a flower, a mite scrambled up your tongue as if it were a ladder. When she reached your face, she crawled through the tangle of your scales and hairs to the outer caverns of your ears; after inspecting both, she chose one and crept inside. Then she stepped up to the delicate membrane—the tympanic membrane—that screens off the inner ear from the outer ear, and she pierced it. In doing so, she destroyed forever your ability to hear with that ear.

  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 popu
lation 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 fru
it—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.