Dr. Tatiana's Sex Advice to All Creation

by Olivia Judson

  Matters have not yet reached such a pass. They are heading in that direction, though. Male rock-boring sea urchins do produce bindin of distinctly different types, and the eggs do have affinities for one type or another. The affinities are not—yet—exclusive. But they will become so if the different bindin-egg interactions continue to diverge. Indeed, such a process seems to have happened before. If you compare yourself with the oblong sea urchin, you’ll see that the biggest genetic differences between the two of you concern those governing the egg-sperm interaction. In other ways, you hardly differ at all. So you see, the rapid evolution of bindin really does have ramifications for your species.

  Curiously enough, in a number of other organisms the proteins involved in reproduction—and therefore in making sperm, eggs, the molecules contained in seminal fluid, and so on—are also evolving fast. Very fast. In mammals, for example, two proteins found on the surface of the egg, both of which interact with sperm during fertilization, are evolving at a gallop. In fruit flies, a protein that influences whether a female’s subsequent lovers will be able to remove a fellow’s sperm, is likewise evolving quickly. But the champion is lysin, a protein that determines whether an abalone sperm can enter an abalone egg: it’s evolving as much as twenty-five times faster than gamma interferon, a protein important in the immune systems of mammals and one of the fastest-evolving mammalian proteins yet discovered.

  This gives us two intriguing facts. First fact: many proteins involved in reproduction are evolving unusually rapidly. Second fact: changes to such proteins can be instrumental in the origin of new species. Putting the two together: if only we knew why proteins involved in reproduction evolve so rapidly, we could gain great insight into the forces underlying the origin of species.

  One reason that proteins involved in reproduction evolve so fast may be the battle of the sexes. It’s certainly an attractive theory—males and females locked into the battle of the sexes are, as we’ve seen, engaged in a fast-moving evolutionary arms race. Moreover, in insect groups where most females mate with more than one male—the precondition for war—new species arise at least four times faster than in groups where most females mate only once.

  This finding is an encouraging start, and bodes well for the theory. It is too early, however, to leap to any definite conclusions. To show that the battle of the sexes is driving the origin of new species, we would ideally want to show that rapid evolution in a given male reproductive protein is fueling the rapid evolution of a given female reproductive protein, and vice versa. To give a hypothetical example, suppose that sea urchin sperm are evolving to penetrate the egg ever faster. From the egg’s point of view, this is bad news: faster penetration may mean that more than one sperm succeeds in entering the egg. But the egg doesn’t “want” to be entered by more than one sperm, since in your species more than one sperm prevents the embryo from developing. Therefore, an egg that resists being penetrated too rapidly could have an advantage. To date, though, we have only one example of a fast-evolving protein where both sides of the story are known, and the results are something of a cautionary tale: it’s more of a chase than a war.

  As I said a moment ago, lysin, the protein that determines whether an abalone sperm can enter an abalone egg, is evolving at record speed. Tantalizingly, abalone are also splitting into new species at a startling rate. So let’s look at what’s going on with the egg. Like sea urchins, abalone release eggs and sperm into the water by the thousands. Each abalone egg is enveloped in a fibrous substance called vitelline. In order to enter an egg, the sperm must break a hole in the vitelline; the breaking is done by lysin. Thus the lysin carried by the sperm must first be able to attach to the envelope of the egg. Changes to the envelope, therefore, may make it harder for lysin to attach. If lysin cannot attach properly, the sperm carrying it cannot get inside. Therefore any changes to the envelope should quickly be matched by changes to the lysin carried by the sperm.

  It turns out that lysin is indeed evolving in response to the egg. The egg, however, is not evolving in response to lysin. Instead, the envelope changes by accident, and lysin races to keep up. This is puzzling. Lysin evolves at record speeds while the egg drifts nonchalantly along? The key to the mystery lies in the nature of the egg’s envelope. It is a complex entity, a mosaic of several components. The particular bit of it that lysin attaches to is a giant molecule called VERL—vitelline envelope receptor for lysin. It is made up of one unit repeated twenty-eight times.

  Repeated units often create genetic problems. For example, suppose a gene contains a stretch where the same letter, or pair of letters, of the genetic alphabet is repeated several times in a row. When the time comes to copy the gene—for example, when making eggs or sperm—the genetic copying machinery of the cell slides along the DNA molecule, making a replica of the gene as it does so. All goes well until the copying machinery comes to the repeats. Then, all too often, the machinery slips, loses its place, and accidentally puts in too many repeats or too few. It’s as if you were trying to copy the number 7878787878787878787 without punctuation marks and without being able to go back and check it. And yes, this can wreak havoc. Several human genetic diseases—the dementia known as Huntington’s disease, for example—are caused by accidental changes in the number of repeats.

  In the case of abalone’s VERL, the unit that is repeated is big—rather than starting again every second letter, it starts again every 460th letter—so slippage isn’t the problem. But something else peculiar can happen. When a repeated unit is large, a mutation that occurs in one unit may spread gradually through the other units through a passive process known as concerted evolution. Exactly why this happens is not well understood. But it can have serious consequences. Suppose that a mutation occurs in one of VERL’s twenty-eight units. And suppose the mutation is so severe in its effects that the unit is unrecognizable to lysin. From the egg’s point of view, this is irrelevant. The other twenty-seven units of each VERL molecule will still function, so the mutation won’t affect the egg’s chances of being fertilized. Initially, this won’t make any difference from the sperm’s point of view either since the sperm will be able to find an unmu-tated unit to attach to. But if the mutation starts spreading through the other units, then any male who produces a version of lysin that can recognize the new unit will start to have an advantage. And I’m afraid it is this passive process that seems to be driving lysin’s extraordinarily rapid evolution—and causing abalone to split into new species. Rather than a battle, abalone is engaged in an evolutionary pursuit.

  This result doesn’t invalidate the idea that the battle of the sexes may be an important cause of the origin of species. It simply means that we have to be careful not to jump to conclusions until we have more data. As for sea urchins, I’m afraid that little is known about the egg side of matters, so I can’t say yet whether you’re a sex warrior, a skirt chaser, or something else altogether. If I find out, I’ll let you know.

  Dear Dr. Tatiana,

  My son cuts a fine figure of a manatee, and I’m very proud of him. But there’s one problem. He keeps kissing other males. What can I do to straighten him out?

  Don’t Want No Homo in the Florida Keys

  It’s not your son who needs straightening out. It’s you. Some homosexual activity is common for animals of all kinds. Look at the bonobo, a sensual creature also known as the pygmy chimpanzee (which is odd, as it’s no smaller than the regular chimpanzee). Bonobos like sex, and female bonobos like sex with each other. One lies on her back, another climbs on top, and they rub genitalia. Among Adélie penguins, one of the smaller penguins in Antarctica, the males, like most birds, have no penis. But that doesn’t stop a bit of gay jiggery-pokery. In one recorded incident, two males bowed to each other as they would to a female, then one lay down on his front, raised his bill and tail like any coquettish girl penguin, and the other copulated with him, ejaculating into his genital tract. They then swapped roles. Or look at dolphins. The bottle-nosed dolphin is catholic in
its choice of sex partners. Males are frequently sighted copulating with turtles (they insert their penises into the soft tissues at the back of their victim’s shell), with sharks, and even with eels. Eels? Yes, when a dolphin’s penis is erect, it has a hook on the end—and many a male will use it to hook a writhing, struggling eel. So it should be no surprise that males also copulate with each other, inserting their penises into each other’s genital slits. The Amazon River dolphin, or boto, sometimes goes further, penetrating another dolphin’s blowhole. So I wouldn’t worry about a little kissing.

  Why do they do this? Maybe they like it. In the stump-tailed macaque, a gregarious Asian monkey with a (guess what?) stumpy tail, females achieve orgasm through female-female mounting just as they do from heterosexual copulation. Or maybe it serves a social function. Among baboons, homosexual behavior between males seems to facilitate teamwork. Males who mount each other and fondle each other’s genitals are more likely to work together when fighting against other males. Or maybe it has an antisocial function. Among razorbills, northern black-and-white seabirds that resemble puffins, males mount each other as a display of aggression. Male razorbills do not like being mounted; they never solicit it, nor do they cooperate if it happens. Instead, they either fight back or run away. Males who are mounted a lot become intimidated and give up their efforts to compete for mates.

  Or maybe homosexual activity springs from desperation. That’s the most logical interpretation of a copulation witnessed between two octopuses, not just of the same sex (both male) but of different species. These octopuses live twenty-five hundred meters (eight thousand feet) under the sea and presumably meet other octopuses of any sort rather rarely. Almost nothing is known about these particular octopuses: the tryst was the first time that a member of either species had made itself known to science. In general, however, male octopuses do not live long once they mature sexually so, if mates are scarce, perhaps no potential partner should be passed up. And in several species of gull, females are more likely to form pairs with each other when males are scarce. Female couples build a nest together, defend the nest together, and help each other incubate their eggs. But although the girls mount each other and display to each other as they would to male partners, neither adopts a “male” role. In case you’re wondering, the eggs are fertilized by males paired to other females in the colony. Female couples are less successful, hatching fewer eggs and rearing fewer chicks than conventional pairs. It’s better than nothing, however: without some kind of partner, they wouldn’t be able to raise any offspring at all.

  In most species, though, homosexuality doesn’t lead—even indirectly—to reproduction. So it might seem odd that homosexuality should persist. Indeed, among humans, this is taken as proof that homosexuality cannot be genetic. But it can. In fact, from an evolutionary point of view, homosexual behavior is only perplexing if every one of three conditions is met. First, the behavior must have a genetic basis. If there is no genetic basis, homosexuality cannot be subject to natural selection. Second, it must be exclusive. That is, at least some individuals engaging in homosexual behavior must be confirmed bachelors or confirmed spinsters who never attempt to breed. If they breed, it’s no mystery why the genes persist in the population. Third, such individuals must make up a significant proportion of the population. If the behavior is rare, it can be dismissed as a fluke. But if it is common, then there must be something that keeps the genes for homosexuality present at an appreciable frequency even though the individuals expressing the genes never reproduce.

  So, are the three conditions met? With regard to the first, I should say at once that we know little about the genetic basis of homosexual behavior in any organism, let alone manatees. In humans, the search for genes involved in homosexuality has so far been inconclusive. Some studies find a link, others do not. In fruit flies, however, mutations in a number of genes affect a fly’s homosexual proclivities. Some mutations cause males to court males and females indiscriminately. Some cause males to court only males: put several males together, and they will pursue one another in a ring. Bizarrely, one mutation causes males to engage in bisexual behavior only when the lights are on. Extinguish the lights and you extinguish their libidos: these flies don’t like sex in the dark. Of course, it is difficult to extrapolate from fruit flies to humans or manatees. But it seems likely—indeed, I would bet on it—that sexual orientation in mammals will turn out to have some genetic basis.

  As to the second condition, we know even less about the extent to which an individual’s homosexual behavior is exclusive. Among humans today, particularly those in the West, some individuals are undoubtedly exclusively homosexual for their whole lives; the extent to which this has always been true, however, is unknown. Social pressures to marry or leave an heir may have meant that most individuals with strong homosexual preferences reproduced anyway. And in other animals—well, we can’t begin to say. Manatees are not known to develop exclusive homosexual preferences. Among captive Japanese macaques, though, males and females sometimes fight each other to have sex with a popular female. (This monkey reaps the benefits of a long tail: a female often rubs her clitoris with her tail.) In captive rhesus monkeys, males sometimes prefer to have anal sex with each other rather than to copulate with females. Whether, given the choice, such individuals maintain their preferences to the exclusion of breeding is unknown.

  And the final condition—the incidence of the behavior? We have no idea for any animal. Even among humans, measuring the incidence of exclusive homosexuality is tricky.

  But for the sake of argument, let’s assume that, in some species at least, all three conditions are met: homosexuality is genetic, exclusive, and common. What can stop the genes’ disappearance? Or, to put it more formally, how can the genes be maintained in the population?

  The traditional explanation is that the genes can be maintained if homosexual individuals act to increase the reproductive success of their relations. This is because related individuals share a certain proportion of their genes. Identical twins, for example, have all genes the same. A child shares half its genes with each parent. Full brothers and sisters who are not identical twins share, on average, half their genes. (I say “on average” because each gets half his or her genes from each parent, but the halves will be drawn at random.) Similarly, first cousins share, on average, one eighth of their genes. And so on.

  This means that you don’t necessarily have to reproduce to spread your genes. Instead, you can devote yourself to helping your relations spread theirs. Such a calculus often explains apparently altruistic behavior, such as that of the ants, bees, and wasps who slave away for the good of the colony and never reproduce themselves. But there is no evidence that homosexuality amounts to an indirect way of spreading genes; in species of birds and mammals where young animals help their parents raise the next brood, there’s no evidence that the helpers are prone to homosexuality. On the contrary, they typically go on to breed themselves in the following season.

  A variant of this idea draws inspiration from another aspect of animal social life. Among animals that live in highly organized groups, such as termites, snapping shrimp, wolves, and naked mole rats, only a few individuals breed. Everyone else is a nonreproductive worker. At least in the case of wolves and naked mole rats, the reason workers don’t breed is not because they are physiologically incapable of reproducing but because their reproduction is suppressed by the dominant pair. It is possible, in principle, that homosexuality could evolve as a type of reproductive suppression, with homosexual individuals a nonreproductive caste akin to the warriors in a termite colony. The argument would be that for those organisms who must live in groups to survive, natural selection acts on groups rather than on individuals. If groups with homosexual individuals do better, in evolutionary terms, than groups without them, then the trait will be maintained. This could work if, for example, homosexuals engaged in activities that were good for the whole group, such as hunting or fighting to defend the group from raid
s by neighbors. But again, there is no evidence that this explains homosexual behavior in any species. In addition, the idea has a theoretical weakness. Unless groups are also family units—as they are in termites, snapping shrimp, wolves, and naked mole rats—the forces favoring reproductive suppression are likely to be weak. Unrelated individuals, after all, have little reason to cooperate in having their reproduction suppressed.

  Alternatively, genes for homosexuality could be maintained if the genes themselves are favored by natural selection. This could happen in two ways. The first is known as heterozygote advantage. Suppose a given gene has two possible forms. Since you get two copies of the gene, one from each parent, you could have two copies of the first form, one copy of each, or two copies of the second form. Geneticists say there is a heterozygote advantage when having one copy of each is better than having two copies of either one. The textbook example is resistance to malaria in humans. The molecule that carries oxygen around the body in the bloodstream, transported in red blood cells, is hemoglobin. A variant of the hemoglobin gene, known as sickle cell, causes the hemoglobin molecule to take the wrong shape once it has released its oxygen, causing the red blood cell to collapse. If you have two copies of the sickle cell gene, you’ll have severe anemia—and without intensive medical treatment, you won’t live long. But if you have only one copy of the sickle cell version of the gene, you are resistant to malaria. The only drawback—and it is a severe one—is that two parents, each immune to malaria, risk one child in four’s dying of sickle cell anemia.