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1: Before Parasites Were Cool It’s not easy being a parasite. Sure, you get a free meal. But the life of a moocher still comes with plenty of stresses. You have to be able to adapt to the environment inside one, two, or, if you belong to a class of parasitic worms known as trematodes, three different hosts—habitats that can be as different from each other as the Earth is from the moon. And getting from one to the next can be a logistical nightmare. Imagine you’re a trematode, a microbe that spends its adolescence inside an ant but can reach full maturity only inside the bile duct of a sheep. Ants aren’t on a sheep’s normal menu, so how do you make it to your next destination? The answer to that question is what set Janice Moore on her life’s path. In 1971, she was a senior at Rice University in Houston sitting in an introductory course on parasitology taught by a titan in the field, Clark Read, a lanky man with a commanding presence and an odd style of lecturing. He would puff away on a cigarette and seemingly free-associate, drawing students into his passion with fascinating details about different species of parasites that he presented with no discernible regard for logic or order. But he was a gifted storyteller who could evoke the lives of parasites so richly that you could almost picture what it was like to be one. He also knew how to spin a good mystery, which was how he ensnared Moore. She couldn’t imagine how to get an ant into a sheep’s mouth in spite of Read’s admonishment to “think like a trematode!” In fact, no one could, because the solution the parasite lit upon is absurdly improbable: It invades a region of the ant’s brain that controls its locomotion and mouthparts. During the day, the infected insect behaves no differently than any other ant. But at night, it does not return to its colony; instead, it climbs to the top of a blade of grass and clamps onto it with its mandibles. There, it dangles in the air, waiting for a grazing sheep to come by and eat it. If that doesn’t happen by the next morning, however, it returns to its colony. Why doesn’t it just stay attached to the leaf? asked Read, scanning the classroom as if he expected his students to discern the trematode’s logic. Because otherwise, he told his rapt audience, the ant will fry to death in the noonday sun—an undesirable outcome for the parasite, which will perish with it. So up and down the ant goes, night after night, until an unsuspecting sheep eats the ant-laden blade of grass, and the parasite finally ends up in the sheep’s belly. Read’s tale stunned Moore. The trematode called to mind a comic-book arch villain who controls minds with a joystick, causing law-abiding citizens to rob banks and commit other crimes so the villain can take over the world. The report of the trematode’s astonishing feat came from a German study done in the 1950s, but, thrilling Moore, Read had just learned of research being done on a different organism that was producing findings similar to the Germans’. The protagonist of this tale was a thorny-headed worm—a parasite with a spiky head and a flaccid body that looks like a five- to ten-millimeter worm-shaped sac. Before assuming its adult form, the parasite must mature inside tiny shrimplike crustaceans that live in ponds or lakes and that usually burrow into mud at the first sign of trouble. For the next stage of the worm’s development, however, it needs to get inside the gut of a mallard, beaver, or muskrat—all creatures that live on the water’s surface and feed on the crustaceans. To determine how the stowaway manages to jump ship, John Holmes, a former student of Read’s who had become a professor at the University of Alberta, and his graduate student William Bethel brought crustaceans into the lab. Infected ones, they discovered, did exactly what they shouldn’t. Instead of diving downward when agitated, they shot to the surface and skittered around, all but crying, Look at me! If that failed to draw attention, they clung to vegetation that waterfowl and aquatic mammals liked to eat. Some, Moore was amazed to learn, even attached themselves to the webbed feet of ducks and were promptly swallowed. Another intriguing detail grabbed her attention. Occasionally, the Canadian investigators found, the crustaceans harbored a different species of thorny-headed worm. When infected with this variety, their tests showed, the crustaceans also swam upward in response to any disturbance, but they congregated in well-lit areas frequented by scaup (deep-diving ducks)—as it turned out, that particular parasite’s next host. Many interactions between predators and prey, thought Moore, were not what they appeared to be but rather were “rigged” by parasites. Perhaps biologists, who couldn’t see what was happening out of view, had been hoodwinked! What’s more, if parasites were not just swinging a sledgehammer, directly killing and sickening hosts, but also bringing ill upon them by subtly changing their behavior, the ecological implications were enormous. It meant that these tiny organisms were taking animals out of one habitat and putting them in another, with unknown effects that would ripple through the food chain. When the class ended, she rushed up to Read. “This is what I want to study,” she announced, brimming with excitement. He applauded her decision as an adventurous one and they hatched a plan for her future. You’ll need to get a master’s in animal behavior and then you should get a PhD in parasitology, he advised, and she did exactly that. Four decades later, she looked back on that day with amusement. “I was bright-eyed, enthusiastic, and totally ignorant of the obstacles in the way,” she said, breaking into a deep-throated laugh at the thought of her youthful optimism. Vivacious, with short wavy hair, Moore still has a trace of a Texan twang and she has a vibrant, confident style. Now a professor of biology at Colorado State University, she has arguably worked harder than anyone else to awaken the biology community to the game-changing nature of parasitic manipulations and encourage a new generation of scientists to take up that cause. Her pioneering studies—and, more important, her writings—have shone a spotlight on the myriad ways parasites bend hosts to their will and on their subversive, often underappreciated role in ecology. Predators, in her view, may not always be the supreme hunters nature documentaries suggest they are. A significant portion of their catch of the day may be low-hanging fruit brought within their reach courtesy of parasites. Why, after all, work hard for a meal when it will come to you? Perhaps the most heretical notion of the field she helped found is simply that one should not assume animals are always acting of their own volition. Numerous crustaceans, mollusks, fish, and “literally truckloads of insects,” according to Moore, “are behaving weirdly because of parasites.” Mammals like ourselves appear to be less common victims of their manipulations, but that belief may derive from ignorance, she cautioned. This much she’s certain of: An undiscovered universe of animal behavior will yet be traced to parasites. Their meddling, in her view, is just harder to prove in some species than others. Moore and a growing cadre of like-minded scientists are making progress in their mission, but it’s been a long haul—as the reason for our first meeting in the spring of 2012 underscored. We’d both traveled thousands of miles to a bucolic corner of Tuscany, Italy, to attend the first-ever scientific conference devoted solely to parasitic manipulations. Sponsored by the prestigious Journal of Experimental Biology, the historic event drew a few dozen researchers from all over the world—a tribute to how far the discipline had come but also an occasion to reflect on how much further it would have to go to attain a stature commensurate with its importance.
