Dr. Tatiana's Sex Advice to All Creation

by Olivia Judson

  With respect to California mice, I can’t say much more than that. In the case of your rival for the title of Ultravirtuous Rodent, the prairie vole, though, scientists are starting to figure out the genetic basis of monogamy. So let’s take a brief look at what’s been discovered about how it works in males.

  When a boy prairie vole meets a girl prairie vole and they decide to become an item, they consummate their relationship by copulating anywhere from fifteen to thirty times in twenty-four hours. From this point on, the lovers grow greatly attached, endlessly cuddling and grooming each other, the picture of mushy affection. And that’s not all. Before losing his virginity, a male is a peaceful sort of chap, not prone to picking fights; but after his first night of passion his personality changes. Now if he sees any prairie vole—male or female—who is not his partner, he’ll attack vigorously. What accounts for his transformation?

  Sex. For a male prairie vole, the sex act causes the release of vasopressin, a hormone that binds to special receptors (the vasopressin V1a receptors) in the brain and alters his behavior. We know that vasopressin is responsible because, if you inject a mating male with a chemical that blocks vasopressin from binding to the receptors, he will behave as though he has not had sex. Conversely, if you inject vasopressin into a virgin male, he will behave as though he has.

  Strong stuff. But before any girls out there start dosing their boyfriends with vasopressin, I should say that this trick won’t work on everyone. For although vasopressin is found in all mammals, it has different effects in different species. As proof of this, consider the montane vole, a close relative of the prairie vole. Montane voles mate promiscuously, they do not form stable couples, lovers rarely sit companionably together or groom each other, and sex induces neither affection nor aggression. Inject a male montane vole with vasopressin and he won’t pick fights. He’ll groom himself.

  These different responses to vasopressin appear to be due to the way vasopressin V1a receptors are distributed through the brain—a distribution that differs considerably between the two species. Intriguingly, it’s quite straightforward to create the prairie vole’s distribution. All you need is a mouse embryo and the gene that contains the instructions for building the prairie vole version of the receptor. Combine the two—which gives you a mouse carrying the prairie vole gene—and you’ll get an adult mouse with vasopressin V1a receptors distributed in the prairie vole pattern. Give this mouse a shot of vasopressin and it will start to behave like a prairie vole in love.

  These results give us a glimpse of the underlying mechanism of monogamy; the full story will probably turn out to be much more complicated. Moreover, since monogamy has evolved independently in different species, the mechanisms may well differ from one monogamous species to the next. All the same, if sex also turns out to have potent hormonal effects in other monogamous species, this would explain why many of them—from the Indian crested porcupine to the wood roach Cryptocercus punctulatus—regularly engage in sex that, owing to its timing, cannot possibly result in reproduction. (It’s particularly amazing that porcupines have far more sex than necessary for reproducing—porcupine sex is potentially pretty prickly.) Irrespective of such matters, however, it is important to remember that understanding the genetic mechanisms of monogamy is quite separate from understanding why organisms have evolved to be monogamous in the first place.

  What, if anything, does all this mean for humans? For now, nothing is known about the genetics of human monogamy, but I’d like to indulge in some speculation.

  Taken as a species, humans cannot be described as exclusively monogamous. Divorce rates and extramarital affairs attest to that. Also, nonidentical twins occasionally have different fathers (although how often this happens is unknown since it’s not usually detected unless the fathers come from different ethnic groups). But humans are not wildly promiscuous, either. Some individuals are faithful to one partner for their whole lives; few have or admit to having thousands of sex partners. Moreover, a couple of indices put humans as a whole on the monogamous end of the scale. First, consider physical differences between males and females. In monogamous species, males and females tend to be roughly the same size; in species where a few big males hold harems, males tend to be enormously bigger than females. Remember the southern elephant seal, where adult males are typically twice the length of adult females—and may be as much as ten times heavier? In the gorilla, adult males are typically twice the weight of adult females. In contrast, human males tend to be only slightly bigger than females, and there is considerable overlap, with some women bigger than some men.

  Next, consider physical differences between human males and other male apes. As you know, testicle size is usually associated with the risk of sperm competition. Males that are at low risk of sperm competition—either because they are good at defending a harem or because they are paired with a faithful female—generally have testicles that are small in relation to their body size. Males that are at high risk of sperm competition—either because they pursue a strategy of seducing the partners of other males or because most females mate promiscuously—generally have enormous testicles in relation to their body size. Male gorillas are at low risk of sperm competition and have tiny testicles. Male chimpanzees are at high risk of sperm competition and have gigantic testicles. In comparison, human males have medium-sized testicles, suggesting a low to moderate risk of sperm competition. This fact, plus the relatively small size differences between men and women, is exactly what would be predicted for a mostly monogamous species.

  What about the rate of infidelity as measured by genetic paternity testing? This is always rumored to be extremely high among humans—30 percent or more. But in fact, surprisingly few studies have even looked at it: despite an extensive trawl through the scientific literature, I could find only a handful. Of these, most showed a low rate of infidelity—3 percent or less; the highest value I found was 11.8 percent. These results need to be treated with more caution in humans than in other species: contraception and abortion enable humans to avoid having a child during an extramarital affair. In the past, however, these would have been less of a factor, and there are ingenious ways to get at historical infidelity. For example, in England, children usually get their last name from their father. Boys get something else from their father: their Y chromosome. Thus, if all living males bearing a particular last name are the direct descendants of one man, they should all have the same genetic markers on their Y chromosomes. In the absence of infidelity (or adoption), last names and Y chromosomes should match up. One study analyzed the Y chromosomes of men called Sykes, a name that first appears in written records about seven hundred years ago. It turns out that almost all the Sykeses investigated did indeed have the same markers on their Y chromosome, suggesting that most living Sykeses have the same distant ancestor. The rate at which females married to Sykeses were unfaithful (or adopted sons) over the period of seven hundred years is estimated to be 1.3 percent per generation. But maybe there’s something odd about Sykeses. It would be great to have more studies on other names.

  Supposing that humans as a whole are best described as mostly monogamous, we are left with two questions. First, what forces may have led to mostly monogamous humans? There are several possibilities—including, perhaps, cultural pressures. Beyond concluding that more monogamous people must generally have had higher reproductive success than less monogamous people, we cannot say much. Second, do individual humans—just like individual crickets and fruit flies—differ in their genetic predisposition toward monogamy? To put it another way, social mores aside, do some people have a much easier time complying with their wedding vows than others have? It is tempting to imagine that once we know more about the genetics of human behavior we will find not only that different men have different proclivities for monogamy but that a given proclivity goes along with a set of other traits—as, you may recall, it does in the California singing fish and among dung beetles. Perhaps it will turn out, for example, that men wi
th large testicles (anticipating a high risk of sperm competition) are prone to seducing other men’s wives and have difficulty forming lasting bonds whereas men with small testicles (anticipating a low risk of sperm competition) are prone to sexual fidelity and jealousy and turn all lovey-dovey after sex. But for now, this is all conjecture …

  For most boys and girls, wedding rings are made of fool’s gold—real, true love is precious and rare, the confluence of bizarre biological forces. Several factors may contribute to monogamy, but you’ll find that true love works best when it is absolutely MAD.

  PART III

  ARE MEN NECESSARY? USUALLY, BUT NOT ALWAYS.

  Male and female form a fundamental, immutable dichotomy, the front and back of a single coin, her yin to his yang.

  Or do they?

  Actually, he is less essential than she is. That’s right, a species can do without him but not without her. Some species reduce the number of males to the bare minimum. Some get rid of males altogether—and simply don’t bother with sex. What’s more, there’s nothing immutable about the two sexes, nothing preordained about sex roles. Some species even transcend yin and yang: they have sexes, sure, but nothing as boring as females and males. Who? When? Why? How? Read on …

  11

  THE FORNICATIONS OF KINGS

  Within human societies, incest is traditionally reserved for royalty. Other organisms, however, are not so elitist. And guess what? Regular practitioners of incest dispense with males almost entirely. So when is it acceptable—or even desirable—for sex to be a family matter?

  Dear Dr. Tatiana,

  Something terrible has happened. I’m a male mite of the species Acarophenax mahunkai—the scourge of the lesser mealworm beetle. This morning I was, as usual, making love with one of my sisters when my mother’s belly burst. All my sisters wandered off, leaving me alone inside Mom’s corpse. Is this punishment for messing with my sisters? What will happen to me now?

  Aghast in Arkansas

  Bad news: you’re finished. All you can do is stagger about on your eight stumpy legs in the hopes of finding a stray sister so you can mate once more before you die.

  Life’s not fair. Not only have you had your day, but you’re not even really the scourge of the lesser mealworm beetle. That’s your sisters. You’re just an accessory to their crimes. Let me explain. The girls in your family suck eggs—the eggs of the lesser mealworm beetle, to be precise. When a mite sucks an egg, her belly swells up to twenty times its usual size and she becomes a huge balloon with a tiny head and legs—the mite version of a caricature of a grotesquely fat man. Her children—as many as fifty—develop and copulate inside her, then she bursts. The newly emerged female mites seek out any lesser mealworm beetles who have succeeded in hatching and stow away on the beetles’ undersides like so many tiny scabs. The female beetle unwittingly carries this deadly cargo with her when she goes to lay her eggs. (Can female mites distinguish between male and female beetles? I would guess they can, but nobody knows.) Meanwhile, you male mites rarely manage to leave your mother’s body—and die almost before you’ve lived.

  Will you go to hell for having screwed your sisters? Don’t worry about that. Whether or not hell exists, incest is not intrinsically bad. If you could flick through Who’s Who in Nature, you’d find a multitude of organisms who, like you, habitually practice close incest without ill effect. True, it’s not advisable for everyone: among humans, for example, the children of brother-sister or father-daughter matings are likely to be sickly or deformed. But this is not divine retribution for monstrous sin. It’s a simple consequence of genetics.

  Problems with incest are due to recessive genes. What’s a recessive gene? Elementary, dear mite. Humans and most other sexually reproducing organisms are “diploid”: they receive two copies of each gene, one from their mother and one from their father. If the two copies are different, how they interact to influence a trait, such as eye color, varies—but the outcome can be simple, with one copy overriding the other. The overriding copy is known as dominant, the overridden copy as recessive. Thus, the effects of a recessive gene don’t show unless an individual has inherited two copies of it. Such an inheritance can be deadly. Recessive genes are more likely not to work properly, so a double whack can be disastrous, resulting in immediate death or debilitating disease.

  When a recessive gene is rare, however, it can persist unseen because most of the individuals who harbor it will have only one copy. Herein lies the danger of incest. Because family members are genetically more similar to one another than they are to strangers, sex in the family raises the odds of uniting two copies of a harmful recessive gene. The closer the kinship of the lovers, the more genes they will have in common—and the greater the risk that harmful recessives will be expressed in their children. Let me give you an example. A recessive gene lurking in one person in a hundred is seven times more likely to meet its twin in the child of a first-cousin marriage than in a marriage between two strangers plucked at random from a crowd. For the child of siblings, the risk is twenty-five times greater. And that’s when the recessive gene is quite common. If the gene is rare—say, lurking in one person in ten million—the risk for the child of siblings is 2,500,000 times greater than for a child of strangers.

  When “inbreeding depression”—the reduced vigor of inbred children compared with outbred children—is severe, close incest is unlikely to catch on. The reason is simple. Anyone who prefers sex with strangers over sex with family members will have more and healthier offspring. If this preference has a genetic basis, genes for outbreeding will spread. Which may explain why humans and some other mammals avoid mating with those who were around them when they were kids. Children reared on Israeli kibbutzim provide a good example: in the golden age of the kibbutz, children were raised in communal children’s homes rather than in small family groups. As adults they reported, often with regret, having no erotic interest in those who’d been their childhood companions—and out of 2,769 marriages of kibbutz children, none took place between former playmates.

  Given all this, you’re probably wondering how—and why—anyone ever gets involved with their siblings, children, or parents. Well, several factors can reduce the severity of inbreeding depression or otherwise tip the balance in favor of incest. Broadly speaking, regular practitioners of close incest fall into two groups. In one, you have hermaphrodites—committing the most intimate incest of all, self-fertilization. (Selfing isn’t as much fun as it sounds: it doesn’t usually involve copulating with yourself. Instead, eggs and sperm shuffle around inside you. But there are exceptions. The earthworm Dendrobaena rubida folds on itself, pressing its male parts against its female parts.) The other group of habitual inbreeders is made up of organisms, such as you, my mitey friend, that routinely bed their nearest and dearest. Joining you in these bacchanalian festivals of the family are the (human) royalty of Hawaii, ancient Egypt, and Inca Peru, many other mites, a few pinworms, and a profusion of insects. Otherwise, recurrent, close incest is rare. So what makes these groups special?

  Consider hermaphrodites first. Roughly 80 percent of flowering plants are hermaphrodites, either making perfect flowers—flowers with both male and female parts—or making separate male and female flowers simultaneously. Of these, perhaps three-quarters self-fertilize once in a while, but far fewer self-fertilize exclusively. Among animal hermaphrodites, much less is known about the proclivity for selfing, but what is clear is that many don’t—indeed, can’t. Upon reflection, this is not surprising: no one is more related to you than you are to yourself, so the offspring of a selfing hermaphrodite are even more vulnerable to inbreeding depression than the fruits of a sibling union. But any child is better than none, and a hermaphrodite who cannot find a mate should eventually switch to selfing, even if the inbreeding depression is appreciable—a strategy I call “emergency selfing.” The white-lipped land snail, for example, prefers outcrossing, but if no mate has appeared after about a year, a lone snail will give up the wait a
nd start selfing. For hermaphrodites, then, the inclination to self-fertilize should depend on the balance between inbreeding depression and the opportunities for mating with others.

  Let’s turn now to nonhermaphrodites. Among the Hawaiians, the ancient Egyptians, and the Incas, brother-sister mating was believed to be a mark of divinity. According to Egyptian mythology, Geb, the god of the earth, married his sister, Nut, the goddess of the sky, while the Incas, who also worshiped incestuous deities, believed that the sun married his sister, the moon. The royal families of both societies claimed divine ancestry—and mimicked their ancestors’ behavior. In old Hawaii, if a chief of the highest rank married a full sister, their son was considered holy and anyone who came into his presence had to lie down. (The unfortunate fellow was apparently confined to his house during the day so that ordinary people wouldn’t have to keep dropping everything and falling flat on their faces to worship him.) If the big chief merely married his half-sister, however, the child was considered less awesome: people had only to sit before him.

  Mythology notwithstanding, it’s worth asking why such practices began and then why they didn’t die out as imbeciles and cripples ascended the thrones. The historical record is silent on the latter point: we don’t know the extent to which inbreeding depression made itself felt. In all three societies, however, kings had a number of other wives; in the event the sibling union proved infertile or produced an individual unfit to rule, another heir could presumably be selected. As to the origin of the custom, one idea is that sibling mating is a natural consequence of rigid social stratification. In stratified societies, few men are suitable matches for the highest-ranking women. After all, cousin marriages (accompanied by a lesser but still detectable degree of inbreeding depression, such as hemophilia and the Hapsburg lip) were common among European royalty, at least in part for this reason. If women are never permitted to marry men of lesser rank than themselves, there will be times when the only mates available to the top women are their brothers.