Dr. Tatiana's Sex Advice to All Creation

by Olivia Judson

  With respect to homosexuality, the idea would be, again, that a given gene has two forms. Two copies of the first form, and you’re an average heterosexual. Two copies of the second form, and you are homosexual—from a genetic viewpoint, sterile. But one copy of each, and you would have some enormous advantage—for example, you might be a highly fertile heterosexual. To me, this seems an unlikely explanation for homosexuality, for three reasons. First, few examples of heterozygote advantage have been identified. Second, in the malaria example, being a heterozygote prevents you from being dead—which, from an evolutionary point of view, offsets the reproductive cost of having some of your children die. But in the case of homosexuality, it is hard to imagine how, with respect to natural selection, the benefit from being a heterozygote could be large enough to compensate for a certain number of your offspring being sterile. Third, it is unlikely that homosexuality is controlled by a single gene.

  I can imagine one other way that genes for homosexuality could be directly favored by natural selection: through an insidious and fundamental form of conflict between the sexes. Namely, if there are genes that produce homosexual behavior in members of one sex but confer great reproductive success on members of the other. From a theoretical point of view this could work. We know that genes that are beneficial in one sex can spread, even if they are detrimental in the other. Under some circumstances such genes can spread even if the benefit to one sex is small while the detriment to the other is large. Thus, suppose a gene causes exclusive homosexuality in males but unusual fecundity when it occurs in females. The gene could persist—and perhaps even spread—despite its reproductive disadvantage in males. The more genes are involved, the more plausible the mechanism becomes. It would also then follow that male homosexuality and female homosexuality are due to different sets of genes.

  But forget theory. What about data? Although the results do not pertain explicitly to homosexuality, there is experimental evidence that sets of genes beneficial in one sex can be highly detrimental in the other. As usual, the study animal was the fruit fly Drosophila melanogaster. Using the latest genetic wizardry, scientists were able to arrange for eggs from different females to be fertilized by males bearing genetically identical sperm. When the eggs hatched, all the fruit flies, both males and females, thus had one set of genes in common and one set of genes different. Comparing these flies with ones drawn at random from the regular population, the scientists were able to evaluate whether possessing a given set of genes is beneficial, first with respect to succeeding as a larva (measured by whether you make it to adulthood), and then with respect to succeeding as an adult (measured by how many offspring you have).

  The scientists tested forty different sets of genes. The results were striking. First, the sets of genes that help you succeed as a larva are beneficial whether you’re male or female. This makes sense: the demands of larval life are the same regardless of your sex. For adult flies, however, the sets of genes that confer success on males turned out to be different from those that confer success on females. Indeed, genes beneficial in one sex are detrimental in the other—and the greater the benefit, the greater the corresponding detriment.

  These results suggest that the mechanism I outlined to explain homosexuality is at least plausible. Beyond that, however, the possibility that genes beneficial in one sex are detrimental in the other suggests that whether you are a fruit fly, a human, or a manatee, the battle of the sexes is inescapable, insoluble, an eternal war.

  Girls, when you jilt one beau and go to bed with the next, pause for a moment to consider the countless ramifications, the evolutionary mischief that may result from your lust. As you fall asleep in his arms, picture the various weapons at work and imagine their gradual refinement over the millennia. Ponder whether you and your men are inadvertently playing a part in the slow creation of new species and pray that your genes are well suited to your sex. For the only creatures who can hope to be exempted from this war are the rarest of the rare: the truly monogamous. We turn to them in the next chapter.

  10

  TILL DEATH DO US PART

  Real happily-ever-after, till-death-do-us-part romance is almost unheard of in nature. Who has it—and under what circumstances does it evolve?

  Dear Dr. Tatiana,

  My husband and I have been faithfully married for years, and we are shocked by what we read in your columns. As black vultures, we engage in none of the revolting practices you advocate so regularly, and we don’t think anyone else should either. We suggest you champion fidelity or shut up.

  Crusading for Family Values in Louisiana

  Remember: revulsion is in the belly of the beholder. And if I may say so, gorging on carrion is considered revolting in some circles. You complain, however, that I do not often urge or even discuss monogamy. I’ll be frank. True monogamy is rare. So rare that it is one of the most deviant behaviors in biology.

  Let me remind you of a few facts. Before the 1980s, more than 90 percent of bird species were believed to be monogamous at least for the duration of the breeding season, and many couples were thought to mate for life. But better genetic techniques and the spread of paternity testing exploded that idea. The halos rolled away like hoops—and not just from birds. Closer inspection of other famously monogamous groups, such as gibbons, revealed that they, too, are not the saints they seemed to be. Nowadays, if animals live in pairs, they are said to be socially monogamous—a term that makes no assumptions about their sex lives. And the discovery of true genetic monogamy is headline news.

  So who’s making headlines? Genetic testing has revealed a scattering of species, like yours, where couples appear to stay faithful. I say “appear” because few studies have covered more than one breeding season or more than a few dozen families; additional information could change the picture. But with that caveat, genetic data support the claims of the jackdaw, a bird that looks like a small crow with a gray skullcap, to be truly monogamous. The chinstrap penguin appears beyond reproach, as does the long-eared owl. Kirk’s dik-dik, one of the smallest African antelopes, seems to have a good case. The California mouse has an excellent reputation. Some termites are devoted lovers. Yet apart from their unusual loyalty, these groups have nothing obvious in common. So let’s take a step back and consider when true monogamy, the real thing, boy and girl together forever, might evolve as a stable strategy for all members of a population.

  The short answer is that monogamy will evolve as a strategy for all members of a population only when it is in the best interest of both males and females. That is, monogamy will be stable only when members of loyal partnerships have more surviving children than fickle creatures do. Lasting fidelity is rare because it’s seldom in the interest of one of the parties, never mind both.

  The usual explanation for monogamy in a species is that a female cannot rear offspring alone. In this scenario, which I call the Good Wife Theory of Monogamy, opportunities for males to philander are predicted to be curtailed by female virtue: would-be philanderers will be unable to find partners because each female will be obsessively faithful to her mate for fear of losing his help with the kids. In other words, monogamy is a female plot forced on males.

  The theory is unlikely, however, to apply widely. In the first place, it assumes that the male would gallivant if he could—and that being faithful is not actually in his interest. But as we shall see, that assumption is often wrong: sexual fidelity can be in the male’s interest. Second, monogamy can evolve even if the male does not help the female raise the children. Look at Kirk’s dik-dik. The buck does nothing to help his mate; he just trots after her wherever she goes. He’s not even any use at detecting predators that could endanger his calf. The African hawk eagle can pick off a baby dik-dik but not an adult, yet only the female reacts to the eagle’s cries.

  The third problem with the Good Wife Theory is that a female’s need for male help does not necessarily guarantee her fidelity. Take the fat-tailed dwarf lemur. No bigger than a squirrel, this
tiny nocturnal primate lives on the island of Madagascar. For the seven months of the dry season, fat-tailed dwarf lemurs hibernate, curled up in tree holes. Like other hibernators, they fatten up before turning out the lights; they store the fat in the base of their tails. In the days before DNA tests, they would have been held up as models of monogamy. Males and females live together in pairs: they snooze together during the summer days, and the male helps with the kiddies, baby-sitting while the female is resting or gathering food. Females cannot raise offspring on their own. Yet genetic testing shows that infidelity is rife, with males often helping to raise children who are not theirs. Of course, this doesn’t mean there’s never an association between sexual fidelity and parents cooperating to look after the young. But as we shall see, when fidelity and cooperation go together, monogamy is typically the cause and not—as the Good Wife Theory would have it—the consequence.

  Let’s look now at other, more plausible ways monogamy can evolve. Suppose females are few and far between. Then, a male who finds one may be better off staying with her and keeping rivals away. Indeed, if females are scattered across the landscape, either of two factors may make long-term monogamy particularly attractive for a male. The first is if it is risky to leave—if, say, finding another girl would entail a long or dangerous journey. The greater the risk, the greater the incentive to remain. I call this the Danger Theory of Monogamy. The second factor is if the time between a female’s broods is short. There may be no point in setting off on a journey, whatever the risk, if your girl will soon be ready to breed again—this is the Pop-’Em-Out Theory of Monogamy.

  The mantis shrimp Lysiosquilla sulcata, an animal that ambushes passing fish by spearing them on its fearsome front limbs, is a fine example of how danger can encourage lasting love. Although the genetics of this case have not been investigated, circumstantial evidence for monogamy is strong. Animals pair up as adolescents, then each couple digs a burrow in a sandy spot on the seafloor. Since these mantis shrimp hunt from the burrow’s concealed entrance—one of the pair lies in wait, only its eyestalks poking out—individuals need never step outside. Indeed, leaving the burrow is almost certainly a death sentence. Whereas mantis shrimp of most species are covered by armor plates, Lysiosquilla sulcata are not. Instead, they have soft bodies—great for burrow dwelling but hopeless against predators. And even supposing an individual managed to roam the seabed without being eaten, building a new burrow would be impossible. To prevent the burrows from collapsing, these animals stabilize the sand with a mucus they produce; as adults, they lose the ability to produce the mucus, so any mantis shrimp wanting out of a relationship cannot simply leave the burrow and build another. Thus, regardless of whether domestic bliss has soured into loathing, it’s better to stay than to go.

  Now let’s turn to another example. Why should a girl tolerate some oaf hanging about? Well, one way for boys to ingratiate themselves is to give her a hand. If a female gains significantly from having a male around, she may be less likely to throw him out. For example, he could help her defend her territory. Or he could help her with child care. The male Djungarian hamster makes himself useful in just this way. Djungarian hamsters live in arid parts of Mongolia. They forage for seeds, which they stuff into pouches in their cheeks; on arriving back at the burrow, they unload their cargo by pushing on the pouches with their forepaws so that seeds stream forth. The male is such an attentive father that he plays the midwife for the births of his pups (the only male mammal so far known to do this as a matter of routine), helping them emerge from the birth canal, opening their airways so they can breathe, and licking them clean. For good measure, he eats the placenta, a delight usually reserved for the female. Consistent with the Pop-’Em-Out Theory, female Djungarian hamsters live apart from one another: their ranges do not overlap. And they are prolific breeders. In a year, they can produce eighteen litters of between one and nine pups each. In contrast, their close relative the Siberian hamster breeds for only a few months of the year and exhibits neither paternal care nor monogamy.

  Are there any other ways monogamy can evolve? Certainly. Monogamous organisms are often aggressive toward any animal who’s not their partner; it’s usually thought that they are aggressive because they are monogamous. But sometimes they may be monogamous because they are aggressive. Suppose that individuals who are aggressive toward members of their own sex have more surviving offspring than more amiable creatures. Then monogamy may arise as a side effect of that aggression. This is the Sociopath Theory of Monogamy. As a possible example, consider banded shrimp. These animals look like candy, with long white antennae like spun sugar, their bodies and claws white but encircled with big red bands. They typically live in twos, feeding each other and standing guard while their partner molts. Each member of the pair, however, is ferociously aggressive toward shrimp of its own sex and will fight such individuals to the death. I know people like that.

  Alternatively, monogamy may arise when cheating or desertion by either partner results in total reproductive failure for both. This is the Mutually Assured Destruction, or MAD, Theory of Monogamy. One group thought to be MAD lovers are hornbills—birds found throughout Africa and Asia. Hornbills come in various shapes and sizes—there are around forty-five species—but are easily distinguished from other birds by their large, curved bills, which are betopped with a horny casque. Again, even without genetic evidence, the case for monogamy is strong. In many of these species, males and females are completely dependent on each other for the survival of the brood. At the start of the breeding cycle, she climbs into the nest hole and either she or her mate seals the entrance so that only her beak can poke out. The male then feeds her while she lays her eggs and incubates them; once the chicks have hatched, he brings food for the whole family. It’s a demanding job: in the wreathed hornbill, for example, the female may remain inside the nest for as long as 137 days. She molts her flight feathers shortly after she starts to lay eggs, so if he should disappear, all the nestlings and the female will die. Contrary to what one might imagine, this arrangement has not evolved as a trick to prevent the female from cheating; rather, it seems to be a defense against nest predators.

  But not all monogamous organisms kill members of their own sex whenever they meet one, sequester themselves or their partners in tree trunks for weeks on end, live scattered across dangerous landscapes, or produce wagonloads of offspring. Jackdaws, for example, often live in colonies, where opportunities for seducing the neighbor’s spouse are abundant. Yet they don’t seem to take advantage. The reasons for their self-restraint aren’t clear, but I’d guess there’s an element of MADness. Baby jackdaws are difficult to raise successfully: in bad years, 80 percent of couples fail to fledge young. This suggests that both parents must devote all their energies to the nesting effort; anyone wasting time philandering will definitely see the nest fail. There may also be an element of experience. In species that live for many years—and jackdaws do—working with a familiar partner can greatly enhance reproductive success. Among Bewick’s swans, for example, the longer a couple has been together, the better they’ll be at raising cygnets.

  And black vultures? Well, black vultures do tend to nest apart from one another and are fiercely territorial when it comes to protecting the nest. But that can’t account for their fidelity, as they still have plenty of opportunity to encounter potential lovers. While one of the pair is sitting on the eggs, the other will go off foraging—and black vultures often meet up at carcasses or even at roosting sites. But it seems that these birds have a social convention that helps individuals stay faithful. Apparently, black vultures insist that sex be conducted in the privacy of the nest and won’t tolerate lewd behavior in public. If a young bird who doesn’t know better tries to get laid at a roost, the poor creature will be roundly attacked by the other vultures in the vicinity. Who’d have thought black vultures would be so prudish?

  Dear Dr. Tatiana,

  Like, what’s the deal? I’m a sleek young California mouse a
nd am so in heat. But, like, the guy next door won’t pay any attention to me? Even though his wife is totally old and ugly? No way is he still in love with her. How come he’s, like, such a dull dude?

  So Bummed Out in Berkeley

  However old and ugly their wives, male California mice are not to be lured away from them. Once one of these dudes, as you call them, has a partner, he won’t cheat on her even if he finds himself locked up with a virgin in heat. So if you want a man, you’ll have to find one who’s single. Bad luck.

  But perhaps you’re wondering what accounts for your neighbor’s saintly behavior. Well, I guess that infidelity is just not in his nature, that he’s a breed of anti-Lothario. It’s easy to imagine how he could have got that way. These days, California mouse couples are truly monogamous, living together faithfully until one of the partners dies. If you look at their near relatives, however, you’ll find all sorts of lascivious goings-on, so it’s safe to assume that these virtuous rodents are descended from promiscuous ancestors, ancestors who squeaked their bawdy way from one bed to the next.

  If you’ve been reading my columns, you’ll know that a population can only evolve from promiscuity to monogamy if incorruptible couples consistently have more surviving children than libertines do. If this happens, and if monogamy has a genetic basis, then genes associated with monogamy will spread. Eventually, everyone in the population will have these genes. (Note, however, that the genes influencing fidelity need not be the same in males and females.) So it’s possible—indeed, I’d say probable—that your mouse dude has a powerful genetic predisposition toward monogamy.