As luck would have it, there was a snail in New Zealand that fit Lively’s research perfectly. Named Potamopyrgus antipodarum, the quarter-inch snail lived in most lakes, rivers, and streams in the country. While most populations of the snail were all identical clones, the product of parthenogenesis, some were divided into male and female forms that used sex to reproduce.
Lively set out to see if the habitats of the snails had any influence on how they reproduced. The snails that lived in the streams faced sudden floods, while the ones that lived in lakes enjoyed a peaceful, stable existence. According to the Lottery hypothesis, the snails in the streams should favor sex because they had to survive in an unstable place. According to the Tangled Bank hypothesis, there would be more competition in the lakes for different niches, and the males would be in demand there.
Lively hiked to the high mountain lakes where the snails lived and waded into the waters with his net. He gathered the snails there, and to determine their sex, he cracked open their shells and cut them open, looking for a penis behind their right tentacle. But when he looked inside the snails, he was baffled—they were packed with what looked to him like giant sperm. “I showed them—unfortunately for me—to one of the parasitologists at the university, and he said, ‘They’re not sperm, you idiot, they’re worms.’” The parasitologist explained to Lively that the parasites were flukes that castrated their snail hosts, multiplied, and eventually got into their final host, a duck. In some places, the parasitologist told him, the snails were riddled with the flukes, and in others they were free of them.
The humiliation wasn’t hard to handle, though, because Lively realized that these parasites might let him test a third explanation for the endurance of sex: that parasites were responsible. The idea had been offered up in various forms by various scientists, but most fully in 1980 by an Oxford University biologist named William Hamilton. Hamilton argued that when hosts are faced with the Red Queen, sex can be a better strategy for fighting parasites than cloning.
Consider a bunch of amoebae that reproduce by cloning and that are divided up into ten genetically distinct strains. Let’s say that bacteria infect them and the Red Queen’s race begins. The bacteria come in strains of their own, each adapted to a different strain of host. The most common strain of amoebae are pounded down by their strain of bacteria, and when that strain of amoeba loses enough numbers, the parasitic spotlight switches to a different strain. Because these amoebae clone to reproduce themselves, every new generation of amoebae will be genetically identical with their forebears. The bacteria sweep through the same ten strains over and over again, and after a while, they may drive some of those strains into extinction.
Now imagine that some of these amoebae evolve the means to have sex. The males and females make copies of their genes and join them together to form their offspring’s DNA, and as the genes combine, they get shuffled around. As a result, the offspring isn’t a carbon copy of one of its parents but a new jumble of tier genes. Now the parasites have a much harder time chasing their hosts. Because the genes of the sexual amoebae mix, they no longer come in distinct strains, and it becomes harder for parasites to get a lock on them. The Red Queen still takes sexual organisms for an endless run, but their offspring may have less of a chance of getting infected. And the protection that this diversity brings to the sexual amoebae might give them a crucial edge in their competition with asexuals.
It was an elegant idea, but Lively didn’t actually believe it when he first read about it. “My feeling—and I think it was general—was that it was a very clever idea, but it seemed unlikely to me to be true. The reason is that I just didn’t see much parasitism in the world. If you’re going to have a selective pressure that’s intense enough, it should be something that has big, immediately obvious effects. At least in humans in this country, we don’t see those big effects. And the people doing field biology were mainly interested in competition or predation. There was no tradition in parasites.”
But the fact was that most animals—Lively’s snails included—are rife with parasites. On the outside chance Hamilton might be right, Lively decided to start noting whether or not his snails were infested with the flukes. “The theory for parasites was just being laid by Hamilton in 1980, 1981, 1982, but no one had discovered systems where you could test them. I didn’t know I was dealing with one until I started cracking open these snails. I realized it would be able to address Hamilton’s idea, but if they had been viruses I would not have known it. Here we’re dealing with big honking swimming worms, and anyone can see them under a dissecting microscope.”
It didn’t take Lively long to see a clear pattern. The snails in the lakes were more infected with the flukes than the ones in the streams, and it was in the lakes that there were the most males. The more infested a given lake was, the more males it held. The only hypothesis that could account for all three patterns was the Red Queen: in places where there were more parasites, there was a stronger evolutionary pressure for sex. “I was completely surprised. When I had half the data set I eventually published, I thought, ‘Wow, there’s a trend setting up.’ So I went out and got a lot more data to see if it went away. It didn’t. Adding more lakes didn’t change it—it wasn’t a few lakes that were highly sexual and highly infected.”
Lively published those first results from New Zealand snails in 1987. He has made the study of sex his preoccupation ever since. He’s tested the Red Queen hypothesis in other ways and found more support for it. In 1994, for example, he traveled to Lake Alexandrina on the southern island of New Zealand with his postdoctoral student Jukka Jokela. They gathered snails from both shallow and deep waters. In the shallow waters the snails live alongside ducks, which are the final hosts for the flukes, and the ducks shed the flukes’ eggs there. With so many eggs in the water, the snails are sicker in the shallows than farther from the shore. Lively and Jokela found that there are more males among the snails in shallow water as well, probably as a result of the pressure of parasites. In a single lake, they could see parasites shaping the sex lives of their hosts.
At the same time, Lively has watched other biologists find the Red Queen at work in other species. In Nigeria there lives another snail named Bulinus truncatus, one of the species that carry the blood flukes that cause schistosomiasis. Its sex life is more exotic than that of Lively’s New Zealand snails. Every one is a hermaphrodite, with male and female gonads it can use to fertilize its own eggs and produce clones. But some of them also come equipped with a penis, which they can use to mate with other snails.