The Evolution of Sex

Life is a dance of partners–cold viruses and their sniffly hosts, orchids and the insects that pollinate them, garter snakes and poisonous rough‑skinned newts. But no list of life’s dance partners would be complete without Male and Female. For the vast majority of animal species, the dance between the sexes is essential to their existence.

As vital as sex may be, it is a glorious, glistening puzzle. Why do peacocks drag around such grand tails–but not peahens? Why is it that when Australian redback spiders mate, the male hurls himself onto the female’s poisonous fangs, becoming a meal for her at the end of the act? Why do ant nests contain thousands of sterile female workers, all serving a fertile queen? Why do males always have small, mobile sperm, while females have giant, immobile eggs? Why are there males and females at all?

The answers are to be found in evolution. Sex, biologists now suspect, is itself an evolutionary adaptation. It gives sexual organisms a competitive edge over ones that reproduce without males and females. But while sex may benefit both males and females, it creates a conflict of interest between them. The best reproductive strategy for a male is not the same as the female’s. Over countless generations, this conflict gradually shapes animals in many ways, from their anatomy to their behavior. And the conflict doesn’t end once a male and female have mated. Within the womb and within the family, the struggle continues, until it has shaped even the societies of animals.

Evolutionary biologists have found that the peacock’s tail, sterile ants, and suicidal spiders can all make eminent sense once they recognize the conflict between the sexes. And their success at understanding how animals are shaped by sex naturally raises a thorny question: Are some parts of human psychology the result of the evolutionary pressure of sex as well?

Why Sex?

The question of why we have sex is not one that occurs to most people. We have it because we want children, or because it feels good, or both. But many organisms can reproduce without sex. Bacteria and many protozoa can simply divide themselves in two without the help of a partner. Asexual animals are rare, but they exist. Some species of whiptail lizards in the western United States, for instance, have no males. One female will mount another female, bite her neck, wrap around her like a reptilian doughnut, and otherwise mimic what a male lizard does while mating. Herpetologists suspect that the mounting female makes the other female ovulate. But she needs no sperm to fertilize her eggs. They simply start dividing and growing into embryos. As these clones begin to develop, their mothers return the favor to their pseudo‑mates by playing the part of the male. When the lizards give birth, they produce only females, all of which are identical to their mothers.

Sex is not only unnecessary, but it ought to be a recipe for evolutionary disaster. For one thing, it is an inefficient way to reproduce. In a population of asexual whiptail lizards, every new lizard can bear baby lizards of her own; in a population that reproduces sexually, only half of them can. If sexual and asexual members of a species are living side by side, the asexuals should quickly swamp the sexuals with their explosive birthrate. And sex carries other costs as well. When males compete for females by locking horns or singing, they’re using up a huge amount of energy, and sometimes even putting themselves at risk of being attacked by a predator. “The cost of sex is immense,” says Robert Vrijenhoek of the Monterey Bay Aquarium Research Institute.

By all rights, any group of animals that evolves sexual reproduction should be promptly outcompeted by nonsexual ones. And yet sex reigns. Peacocks show no sign of evolving away their tails; new generations of redback spider males are throwing themselves into the jaws of death just as their fathers did. Meanwhile, only a fraction of percent of all vertebrates reproduce asexually like the virgin whiptail lizards.

Why is sex a success, despite all its disadvantages? Scientists have recently been gathering support for a surprising hypothesis: sex fights off parasites. Parasites take a tremendous toll on their hosts, and any adaptation that helps hosts escape them may become hugely successful. In the 1970s, a number of biologists began building simple mathematical models of the coevolution between parasites and their hosts that suggested it moves in circles, like a deadly merry‑go‑round.

Imagine a pond of fishes that reproduce by cloning. Each fish is an identical copy of its mother, but the fishes are not all carbon copies of one another. A mutation may arise in one fish and be passed down to her descendants. They will form a strain that can be distinguished from other strains by unique mutations

Now suppose a fatal parasite invades the pond. The parasite mutates as it spreads, forming strains of its own. Some strains of the parasite carry mutations that make them good at attacking certain strains of fish. The strain that can attack the most common fish has the most hosts to attack, and it soon becomes the most common of all parasite strains. The other parasite strains, limited to fewer hosts, dwindle to low levels.

But the parasites undermine their own success. They thrive so intensely in their strain of fish (call it Fish A) that they kill their hosts faster than they can reproduce. The population of Fish A crashes, and as it disappears, its parasites have a harder time finding new hosts to infect. Their numbers crash as well.

This attack on Fish A gives the rarer strains of fishes an evolutionary edge. Unburdened by parasites, their numbers swell. Eventually another fish strain becomes most common–call it Fish B. As it grows more successful, it becomes fertile ground for the rare parasites that are best adapted to them. They begin to multiply and catch up with the explosion of their host. Now Fish B crashes, to be replaced by Fish C, and so on.

Biologists call this model of evolution the Red Queen hypothesis. The name refers to the character in Lewis Carroll’s Through the Looking Glass who takes Alice on a long run that actually brings them nowhere. “Now, here, you see, it takes all the running you can do, to keep in the same place,” the Red Queen declared. Hosts and parasites experience a huge amount of evolution, but it doesn’t produce any long‑term change in either of them. It’s as if they’re evolving in place.

William Hamilton, an Oxford biologist, proposed in the early 1980s that sex might bring an advantage to animals struggling through this Red Queen race, because it makes it harder for the parasites to adapt to them. A sexual animal is not a clone of its mother; it carries a combination of genes from both its mother and father. Nor is it a simple blend of its parents’ genes. As cells divide into eggs or sperm, each pair of chromosomes wraps around each other and swaps genes. Thanks to that sexual dance, the genes of a male and a female can be shuffled into billions of different combinations in their offspring.

As a result, sexual fish don’t evolve into distinct strains; their genes scatter throughout the pond’s population, mingling with the genes of other fish. Fish genes that have lost their protective powers against the parasite can be stored away in the DNA of fish that also carry more effective ones. These obsolete genes may later be able to provide more protection against new parasite strains, and they’ll be able to spread once more through the pond’s populations. Parasites can still attack fish that reproduce sexually, but they cannot force them into boom‑and‑bust cycles as dramatic as the ones suffered by their clonal cousins.

The ups and downs through which parasites drive the asexual fish may make their genes deteriorate. For any given gene, some fish will have defective versions and others will have defect‑free copies. Each time the fish go through a crash, there’s a chance that some of the defect‑free fish will die, taking their unblemished genes with them. After enough crashes, the defect‑free genes may disappear completely.

Once a perfect version of a gene disappears from the fish population, it’s unlikely to return. The only way evolution can repair a defective gene is for a mutation to change the faulty part of its sequence. But mutations strike a gene at random, anywhere along its sequence. It’s far more likely that a mutation will just cause more harm to the gene. The Red Queen phenomenon among asexual fish renders more of their genes defective as time goes by. But sexual fish mix their genes together in every generation, so that defect‑free genes rarely disappear for good. The overall quality of their DNA remains high and may even make them more fit than the asexual ones. Their good genes may give them more stamina or the ability to draw more energy out of the insects they eat. Even though they breed more slowly, their resistance to parasites may give them an evolutionary edge over asexual fish.

That was the hypothesis, at any rate, and while it looked promising in theoretical models, scientists needed to test it in the real world. In the 1970s Robert Vrijenhoek discovered one natural experiment among topminnows that live in Mexican ponds and streams. These topminnows sometimes mate with a closely related species, creating a hybrid fish with three copies of genes rather than two. The hybrids are always female, and they always reproduce by cloning rather than by mating. In order to trigger their eggs to grow, they need to get sperm from a male fish, but they don’t actually incorporate his genes into their eggs.

Vrijenhoek and his colleagues have studied the topminnows in several different ponds and streams, and each one gives a different confirmation of the Red Queen hypothesis. Many topminnows are infected with parasitic flukes, which form black cysts in their flesh. In one pond, Vrijenhoek found that the hybrid clones had many more cysts than sexual topminnows. In other words, the clones provided an easier target than the sexual fish, because the parasites could adapt to their immune systems faster. In a second pond where two strains of clones lived, the more common strain was subject to more infections–just as the Red Queen hypothesis predicts.

The topminnows in a third pond seemed at first to contradict the Red Queen hypothesis: the sexual fish were more vulnerable than the clones. But as Vrijenhoek studied that pond more closely, it turned out to be an even stronger confirmation. It had dried up in a drought a few years earlier, and after it had returned, only a few fish recolonized it. As a result, the sexual fish were highly inbred and were thus deprived of the genetic variety that represents the advantage of sex. Vrijenhoek and his colleagues added some more sexual topminnows to the pond to boost the diversity of its DNA. Within two years the sexual fish were immune to the parasites, which had switched to attacking the clones.

Sperm and Egg

The advantages of sex have allowed it to come into existence dozens of times, in many separate lineages of animals, plants, red algae, and other eukaryotes. The first sexual animals probably just sprayed their sex cells (called gametes) into an ocean current and let them struggle to find each other. Although sex has evolved independently numerous times, most gametes look pretty much the same: the egg is big and immobile, while the sperm is a small swimmer. When the sperm fuses to the egg, it unloads only the DNA in its nucleus; its mitochondria and other organelles are blocked from entering.

This arrangement is popular because it works so well. David Dusenbery, a biologist at the Georgia Institute of Technology, has identified the advantages by building a mathematical model of gametes struggling to find each other. In his model both gametes can swim around or remain stationary; they can be the same size or different. Dusenbery finds that gametes are a bit like two people lost in a giant forest at night. If both of them wander around, they will be unlikely to find each other. It is better for one of them to remain motionless and send out signals to the other one.

In the case of people, the signals might be shouts; for gametes, they are powerful odors known as pheromones. The louder people shout, the easier they are to hear. For gametes, shouting louder means producing more pheromones. Dusenbery finds any increase in the size of a gamete makes it able to make many more pheromones, extending the range of its communication. And in fact, it is eggs that send out pheromones to attract sperm, not the other way around.

Of course, an entire search party fanning out through a forest will do a better job of finding someone than a single person. Likewise, one way to increase the odds of contact is to use many sperm instead of one to search for the egg. According to Dusenbery, evolution would favor any mutation that would make a species’ eggs bigger or its sperm more plentiful. It would be able to use less energy to reproduce successfully, because its gametes would do a better job of finding each other; it could survive in places where less efficient forms couldn’t reproduce.

By evolving to bigger sizes, eggs not only could spread pheromones more effectively, but they could store more energy that they would need to fuel their cell division once they were fertilized. The more energy an egg could provide, the less the sperm would need to bring with them. They could become even smaller and more numerous, increasing their chances of fertilizing eggs and propagating their genes. And in the face of shrinking sperm carrying fewer resources, natural selection favored eggs that could supply even more. Over time sperm evolved into little more than mobile crates of genes, while eggs became giant, energy‑rich cells.

As the big‑egg, little‑sperm arrangement evolved, it created a huge imbalance between the sexes. A single man can produce enough sperm in his life to make every woman on the planet pregnant many times over. But each woman ovulates only once a month, and like other mammals, she has to carry her baby inside her for months and nurse it when it’s born. Each birth puts her at risk of dying from complications, and nursing makes her burn tens of thousands of extra calories. The vast reproductive potential of men has to fit through the narrow bottleneck of womanhood.

While a single male of a species may be able to fertilize every female, there are other males who wouldn’t mind doing the same. In many species, this conflict leads to battles among the males. Exactly what sort of battle evolution produces depends on the species in question and its ecology. Northern elephant seals will slam their 2,000‑pound bodies against one another, spraying blood and foam, in order to be the sole mate for a harem of dozens of females. Musk ox bulls will ram their thick horns against one another on the Arctic tundra, and 1 out of every 10 will die of a fractured skull. Even male beetles and flies have evolved antlers of their own that they use to battle for the right to sex.

Female Choice

Competition between males was well known to nineteenth‑century naturalists, Darwin included. It fit into his theory of evolution without much trouble: if males competed with one another for females, the winners would mate most often. If having a slightly thicker skull gave the edge to the winners, more males of the next generation would have thick skulls. A pair of lumps might make the skull even more effective in fighting, and so those lumps might evolve into horns.

But Darwin wondered what the females were doing during these battles. Were they simply waiting passively to be possessed by the winner of a match? The notion of passive females might appeal to some Victorian gentlemen, but Darwin recognized there was a problem with it: it could not account for species in which males do not go mano a mano.

Consider the peacock and his splendid tail. “The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!” Darwin once said. The great fan of iridescent eyes is not essential to Pavo cristatus– the females survive perfectly well without one. A male can’t use its tail to bludgeon another male into submission. In fact, it’s a burden, since it weighs down the peacock when it tries to escape from a fox. Yet despite its drawbacks, male peacocks grow a new set of tail feathers every year to replace the ones they shed at the end of the previous year.

“Darwin had a real problem with peacocks, because they seemed to go against his theory of evolution by natural selection,” says Marion Petrie, a biologist at the University of Newcastle‑upon‑Tyne. “He thought about it a lot and it was several years before he produced his explanation for why peacock trains might have developed. And he had a special term for the process that might have caused the development of the train, which he called sexual selection.”

During the mating season, peacocks will assemble together in groups called leks, drawing females to them with their cries. As soon as a female comes into view, a male will raise his tail and make it shiver. Darwin proposed that peahens judge peacocks by their tails. They find certain kinds of tails attractive and choose to mate with their owners. Whether their choice was based on aesthetics or on some desirable qualities in the peacock, Darwin didn’t say. In either case, by choosing among males, peahens behave like pigeon breeders who select certain pigeons for qualities that natural selection would have ignored in the wild. A fantail pigeon pleases a breeder’s eye; a resplendent peacock pleases a peahen. With each generation, the preference of females brings more reproductive success to males with pleasing traits. In time, Darwin argued, the choices of females could have created something as extravagant as a peacock’s tail.

Sexual selection, as Darwin dubbed this new force in evolution, didn’t win many admirers. Alfred Wallace thought good old natural selection was sufficient. Female birds were drab because they spent their time in nests, he claimed, where they needed to be camouflaged for protection. Extravagant colors might be the normal state of feathers, and male birds–with less need of camouflage–were not subject to the dulling force of natural selection.

For decades most biologists continued to doubt that females had much say in the matter of sex. Only in the past 20 years or so have researchers performed experiments that can show whether females have preferences. It turns out that they have very strong ones strong enough to drive the evolution of the peacock’s tail.

Marion Petrie, for example, demonstrated that peahens have very clear tastes when it comes to peacocks–“Lots of females, where they’ve got free choice amongst several males, will actually approach one male, and he will get a high proportion of females in the population,” says Petrie. And peahens, Petrie has shown, choose those fortunate males on the basis of their tails. Elaborate tails with lots of eyes are more attractive to peahens than less ornamented ones. Peacocks have on average 150 eyes on their tails. By trimming only a few eyes from a peacock’s tail, Petrie could significantly reduce his chances of getting picked. A peacock with fewer than 130 eyes rarely mated at all.

Other biologists have shown that the females of many other species also have strong preferences in their choice of mates. Hens like roosters with big bright combs; female swordtail fish like males with long tails; female crickets like males with the most complicated calls. Since these displays are hereditary, sexual selection could indeed have driven their evolution. And since long tails and bright colors and loud calls all make heavy demands on male animals, there must be a limit to how extravagant they can become. If they pose too much of a survival cost to males, natural selection will put a ceiling on their evolution.

Darwin was always a bit evasive about one fundamental question of sexual selection: Why did a female prefer a particular kind of tail or comb? He simply said that she found it attractive. In 1930 the British geneticist Ronald Fisher rephrased the idea in a more formal way: if female birds find long tails attractive, short‑tailed male birds will have a harder time finding mates. A female who chooses a long‑tailed mate will presumably have long‑tailed sons, and her male offspring will have a better chance of finding mates. Mothers, in other words, just want their sons to look sexy.

But a growing number of scientists now believe that females are not being arbitrary when they pick their mates. They are actually attracted to displays that can reveal a male’s genetic potential.

Females have fewer chances to pass their genes on to the next generation than males, and so evolution frequently makes them much more cautious about their choice of a mate. One powerful threat to a female’s offspring are parasites. Even if a female has good genes for protecting herself from diseases, she will dilute their power in her offspring if she mates with a male with a weak genome.

A female animal cannot send her suitor’s genes to a lab for analysis, but she can detect clues of his fitness in the way he looks or acts. To sing loudly or grow bright feathers, a male can’t be too weakened by his fight with parasites. Exactly what sort of display the males of a species will evolve as a way to impress their females depends on the peculiarities of the species itself. Primates are the only mammals with good color vision, which may be the reason why some primate species are the only mammals who use brilliant reds and blues in their sexual displays. But whatever form a display takes, it has to represent a sincere sacrifice. If females can be fooled by false displays, their offspring will not inherit good genes from their fathers. The attraction of the false display will evolve away into oblivion.

A rooster’s comb doesn’t physically burden the bird like a peacock’s tail does, but it is a sincere sacrifice nonetheless. The comb, like many other male displays, needs testosterone to trigger its growth. But testosterone also lowers the rooster’s immune system. To grow a comb, a rooster must put himself at greater risk of getting sick. Only truly strong roosters can squander their immune systems this way.

Another sincere form of advertising is symmetry. As an embryo develops, it can be buffeted by different kinds of stress. Its mother may not be able to find enough food while she is pregnant, for example, and so the embryo will not have the energy it needs to grow properly. Some animals are genetically predisposed to withstand these assaults and grow up healthy. But in other animals, the choreography of embryonic development gets thrown into chaos by the stress. As a result, they may grow up to be infertile or susceptible to diseases. A female looking for a mate would do well to avoid males with this instability.

Developmental instability leaves its mark on the visible symmetry of an animal’s body. For the most part, an animal’s body is a pair of mirror images. The same intricate network of genes that builds its left side needs to perform precisely the same job on the right. If the development of an animal is disrupted somehow, the exact symmetry of its body may be thrown off. An antelope’s horns may grow to different lengths; a peacock may grow different numbers of eyes on each side of its train. Symmetry may be a badge of fitness.

Researchers are now testing whether females use male displays to judge their genes, and many of their results support the idea. Female crickets prefer males whose songs have extra syllables in them, and the length of a cricket song is a reliable indication of a strong resistance to parasites. Female barn swallows prefer males with long tail feathers that are symmetrical, and length and symmetry are both reliable clues that it is healthy. Marion Petrie has shown that peacocks with bigger tails are more likely to survive than peacocks with smaller tails, and those survival rates get passed on to their offspring.

One of the best ways to test an evolutionary hypothesis is to find an exception that proves the rule. Not every animal species has males competing over display‑judging females. In a few species the roles of the sexes have been partially reversed. The female pipefish (Syngnathus typhle ) places her eggs in a pouch in the male’s body, and the male essentially becomes pregnant. For several weeks he carries the eggs, supplying them with nutrients and oxygen from his own blood. In a single breeding season, each female can make enough eggs for two males to carry, creating a fierce competition among the females for the limited number of available males. As a result it is the male pipefish, not the females, who choose their mates, preferring big, ornamented females over small, plain ones.

When animals choose mates they don’t make conscious decisions. Peahens do not count the eyes on a peacock tail and think to themselves, “Only 130 eyes? Not good enough. Next!” Peahens probably experience a complicated chain of biochemical reactions at the sight of a sumptuous peacock tail that leads them to mate with its owner. Such is the case for most sorts of adaptive behavior: although they are based only on instinct, they can carry out a sophisticated strategy for survival.