As with the New Zealand snails, it seems like a huge waste of effort for the Nigerian species to grow a penis and have sex when it can just fertilize itself. And as in New Zealand, parasites seem to make the effort worthwhile. According to the parasitologist Stephanie Schrag, each year the snails have a penis season. The waters are coolest in northern Nigeria in December and January. The snails use the cool temperature as a cue to produce more offspring equipped with penises—snails, in other words, that can mate with other snails. With more penises, there’s more sex among the snails, and more shuffling of their DNA, and more variation in the next generation. The snails need about three months to mature, so this new sexually produced generation comes of age between March and June. And March to June happens to be the time of year when flukes are at their worst in northern Nigeria. In other words, snails seem to use sex to prepare months in advance for an annual attack of parasites.
The most unexpected support for the Red Queen’s effect on sex has come from parasites themselves. Like their hosts, many parasites have sex, and in 1997, Scottish scientists asked why parasites bother. Like Lively, they looked for a species that isn’t stuck reproducing only sexually or asexually. They chose Strongyloides ratti, a nematode that, as its name suggests, lives inside rats. The females living in the guts of rats lay eggs without any help from males. Once these eggs leave the rat’s body they hatch, and their larvae emerge as one of two different forms.
One form is all female, and it spends its time looking for a rat to penetrate. It gets into the skin of the rat and then glides through it until it reaches the rat’s nose. There it finds the nerve endings that the rat uses to smell, and it follows them into the brain. From there the parasite takes a route—no one knows the details—all the way to the rat’s intestines, and starts making female clones again.
The other form of the nematode hatches from eggs in the soil and stays there. When the larvae mature, they turn into both females and males rather than females only, and instead of cloning they have sex to reproduce. The females lay fertilized eggs, giving birth to a new generation of worms that can penetrate the skin of rats and get back into their gut. In other words, Strongyloides can complete its life cycle with sex or without.
The Scottish scientists decided to see whether a change in the immune system of a rat might influence the kind of reproduction the parasites chose. They put Strongyloides into rats, and the rats mounted an immune response to the parasites. They then gave the rats shots of antiworm medicine to clear the parasites out of their bodies. Now the rats were primed to fight off a second invasion. When the scientists reinfected the rats and the new wave of nematodes began making eggs, the parasites that emerged from them were more likely to be sexual forms. In another experiment, the scientists depressed the immune system of a rat with radiation and then infected it with Strongyloides. They found that the parasites were much more likely to clone themselves than to have sex.
These experiments showed that Strongyloides would prefer to reproduce asexually, but a healthy immune system forces it to have sex. “Your immune system is a sort of parasite of the parasite,” says Lively. Like parasites, T cells and B cells multiply into many different lineages, and the most successful killers get to reproduce themselves the most. Like their hosts, parasites can defend themselves by having sex and diversifying their genes.
All the work that Lively and these other scientists have done on the origins of sex rests on the Red Queen’s shoulders, and yet it has been hard to get a glimpse of the Queen herself. Some researchers who run computer simulations of the struggle between host and parasite have seen her shadow flit across their monitors. In Lively’s own work, he could see her effects only by mapping where the sexual and asexual snails lived—taking a snapshot of her effects at a given instant. But eventually he had studied enough snails to see her work spread across time rather than space.
For five years he and another of his postdoctoral students; Mark Dybdahl, netted snails in Lake Poerua. The snails there were all clones, and most of them belonged to four main lineages. Lively and Dybdahl took a census of the four snail clans each year and watched their populations rise and fall. They took the rarest clones and the common ones to their lab at Indiana University, where Lively now works. There they exposed both kinds of snails to their flukes. They found a huge difference: the parasites had a much harder time infecting the rare snails than the common snails. Here was a central prediction of the Red Queen: that being rare gives an organism an advantage, because parasites are more adapted to the more common hosts.
They then looked at their census of the snails of Lake Poerua over five years. In a given year, they found, there wasn’t much of a connection between the number of parasites infecting a lineage of snails and how big the lineage was. The ones with heavy burdens of parasites weren’t the most common. But with a five-year record, Lively and Dybdahl could look back at the lineages in previous years. When they did, a distinct pattern jumped out. The snail lineages that carried the heaviest burdens of parasites in a given year had been the most common snails a few years before, and now they were declining. The snails had started out rare and had increased their numbers, but eventually the parasites caught up with them and started driving their numbers down. Because it took a while for the evolution of the flukes to catch up with their hosts, the flukes reached their greatest success only after the snails had already started to decline.
For the first time, scientists have been able to see the Red Queen at work, by moving back through time. It’s a method that Alice would have approved of. At one point in her adventures, she lost sight of the Red Queen. She asked the Rose how to catch her, and the Rose replied, “I should advise you to walk the other way.”
“This sounded like nonsense to Alice, but after only occasional glimpses of the Queen in the distance, she thought she would try the plan, this time, of walking in the opposite direction. It succeeded beautifully. She had not been walking a minute before she found herself face to face with the Red Queen.”
Shortly after William Hamilton proposed that parasites drive the evolution of sex, he realized that this idea naturally gave rise to another one. Sex may help organisms fend off parasites, but it brings trouble of its own. Say you’re a hen, and your genes are particularly well suited to fighting off the parasites that the Red Queen has made most common at the moment. You want to have some chicks, but to do that you have to find a rooster, and half of the chicks’ genes will have to come from him. If you pick a rooster that has bad parasite-fighting genes, your chicks will suffer the consquences. It pays for you to be picky about your mates and to try to figure out which roosters have good genes. The rooster doesn’t have to be as picky, because he can make millions of sperm. You, on the other hand, can raise only a few dozen eggs over your lifetime.
Working with a graduate student, Marlene Zuk, at the University of Michigan, Hamilton suggested that females judge male displays to decide how well they can fight parasites. A weak suitor will have to spend most of his efforts fighting off parasites and will have very little resources left over. But a male who can resist parasites will still have enough energy left over to advertise his healthy genes to females. These advertisements, Hamilton and Zuk argued, should be showy, extravagant, and expensive. A rooster’s comb might qualify as just this sort of biological resumé. It serves no particular purpose in the rooster’s survival. In fact, it’s a burden to him, because in order to keep it red and puffy, the rooster has to pump testosterone into it. Testosterone tends to depress the immune system, putting roosters at a disadvantage in fighting off parasites.