Spillover

by David Quammen

  Worobey’s lab received six tubes of frozen blood cells, and Tom Gilbert managed to amplify viral fragments from five. Those fragments, after genetic sequencing, could be placed into context as limbs on another family tree—just as Worobey himself would later do with DRC60 and ZR59, and as Beatrice Hahn’s group was doing with SIVcpz. It was molecular phylogenetics at work. In this case, the tree represented the diversified lineage of HIV-1 group M subtype B. Its major limbs represented the virus as known from Haiti. One of those limbs encompassed a branch from which grew too many small twigs to portray. So in the figure as eventually published, that branch and its twigs were blurred—depicted simply as a solid cone of brown, like a sepia shadow, within which appeared a list of names. The names told where subtype B had gone, after passing through Haiti: the United States, Canada, Argentina, Colombia, Brazil, Ecuador, the Netherlands, France, the United Kingdom, Germany, Estonia, South Korea, Japan, Thailand, and Australia. It had also bounced back to Africa. It was HIV globalized.

  This study by Gilbert and Worobey and their colleagues delivered one other piquant finding. Their data and analysis indicated that just a single migration of the virus—one infected person or one container of plasma—accounted for bringing AIDS to America. That sorry advent occurred in 1969, give or take about three years.

  So it lurked here for more than a decade before anyone noticed. For more than a decade, it infiltrated networks of contact and exposure. In particular, it followed certain paths of chance and opportunity into certain subcategories of the American populace. It was no longer a chimpanzee virus. It had found a new host and adapted, succeeding brilliantly, passing far beyond the horizons of its old existence within chimpanzees. It reached hemophiliacs through the blood supply. It reached drug addicts through shared needles. It reached gay men—reached deeply and catastrophically into their circles of love and acquaintance—by sexual transmission, possibly from an initial contact between two males, an American and a Haitian.

  For a dozen years it traveled quietly from person to person. Symptoms were slow to arise. Death lagged some distance behind. No one knew. This virus was patient, unlike Ebola, unlike Marburg. More patient even than rabies, but equally lethal. Somebody gave it to Gaëtan Dugas. Somebody gave it to Randy Shilts. Somebody gave it to a thirty-three-year-old Los Angeles man, who eventually fell ill with pneumonia and a weird oral fungus and, in March 1981, walked into the office of Dr. Michael Gottlieb.

  IX

  IT DEPENDS

  110

  Finally, let me tell you a little story about caterpillars. This may seem to take us afield from the origins and perils of zoonotic diseases but, trust me, it’s very germane.

  The caterpillar story begins back in 1993. That year, in the tree-shaded town where I live, it seemed that autumn had come early—earlier even than usual for a valley in western Montana, where the cold winds begin blowing in mid-August, the cottonwoods turn color not long after Labor Day, and the first heavy snow often puts a damper on Halloween. This was different. This was June. It seemed like autumn because the leaves were gone from the trees. They had flushed from their buds in May, opening wide and fresh and green; and then, just a month later, they disappeared. They hadn’t succumbed to the natural rhythm of season. They hadn’t turned yellow, fallen, piled up in the gutters as aromatic autumnal mulch. They had been eaten.

  A pestilential abundance of small, hairy larvae had materialized like a plague out of Exodus, stripping the trees of their foliage. The Latinate binomial for these voracious leaf-eaters is Malacosoma disstria, though few of us townsfolk knew that at the time. We used another name.

  “Tent caterpillars,” said the local newspaper, vaguely but not inaccurately. “Tent caterpillars,” said the city parks people and the agricultural technicians at the county extension service, who were answering calls from dozens of concerned citizens every day. The radio said “tent caterpillars” too. And so before long we were all out on the sidewalks, saying “tent caterpillars!” back and forth to one another. In the hubbub, we were too occupied to notice that these particular “tent caterpillars” didn’t build tents. They just gathered and traveled in dense aggregations, like wildebeests on the Serengeti. Their full common name (their official misnomer?) is the forest tent caterpillar; a closely related insect, the western tent caterpillar (Malacosoma californicum) does build tentlike silken shelters. We weren’t interested in such entomological subtleties. We wanted to know how we could kill the damned things before they ate all our lovely urban hardwoods down to stumps.

  It was awesome, in an ugly way. Not every tree was left naked, but many were, especially among the old towering elms and green ashes that stand along the sidewalks, arching their canopies over the neighborhood lanes. It happened fast. The caterpillars did most of their feeding in full daylight or early evening, but later, on those cool June nights, we could stand beneath a great tree and still hear the gentle crackle, like distant brushfire, of their excrement cascading down through the leaves. In the mornings, we would find the sidewalks heavily sprinkled with those poppy-seed globules of dung. Occasionally a lone caterpillar would rappel down on a filament of silk and dangle there mockingly at eye level. On a day of chilly drizzle, too chilly for caterpillar comfort, we could spot them hunkering sociably, high up on a trunk or in a limb crotch, hundreds of fuzzy gray bodies in each pile, like musk oxen huddled against an Arctic storm. Some of us went away for a weekend, leaving the lawn freshly mowed, all seemingly fine, and came home to find that our trees had been defoliated. We climbed up on ladders and sprayed the caterpillars with soapy dishwater from spritzer bottles. We dosed them with bacterial mists or nasty long-molecule chemicals, as variously prescribed by the local garden-store clerks, who knew little more than we did. We called in SWAT-team strikes by the men from Nitro-Green. All of these measures seemed to be marginally effective at best and, at worst, just poisonous and futile. The caterpillars continued to chomp. When it appeared that they might move from ravaged trees to healthy ones, in search of more food, we tried to stop them by girdling the tree trunks with barriers of impassable goo. This was pointless (since, as I learned later, a tent caterpillar generally lives out its larval stage in the tree where it hatched) but reflected our desperation. I watched my next-door neighbor, Susan, muster such hopeful defenses for two giant elms in front of her house, each tree banded at waist height with a circular belt of spray-on stickum, and it seemed like a reasonable idea to me too. But the stuff failed to catch a single caterpillar.

  They kept coming. They had their way. There were simply too many, and the infestation proceeded along its inexorable course. We stepped on them as they forded the sidewalks. We mooshed them wholesale in the streets. They ate, they grew, they molted their tight old skins and grew further. They marched up and down limbs, all over town, treating our trees like celery.

  Eventually they finished eating. They had bulked themselves up to the limits, fulfilled their caterpillar juvenility, and now they were ready for puberty. They spun themselves up inside leaf-wrapped cocoons for a short metamorphic respite, to emerge in a few weeks as little brown moths. The crackling stopped and the treetops, what was left of them, fell silent. The caterpillars, qua caterpillars, were gone. But this vast population of pestiferous insects still lurked over our heads, almost invisible now, like a large gloomy hunch about the future.

  Ecologists have a label for such an event. They call it an outbreak.

  This use of the word is more general than what’s meant by an outbreak of disease. You could think of disease outbreaks as a subset. Outbreak in the broader sense applies to any vast, sudden population increase by a single species. Such outbreaks occur among certain animals but not among others. Lemmings undergo outbreaks; river otters don’t. Some kinds of grasshopper do, some kinds of mouse, some kinds of starfish, whereas other kinds of grasshopper, mouse, and starfish do not. An outbreak of woodpeckers is unlikely. An outbreak of wolverines, unlikely. The insect order Lepidoptera (moths and butterflies) conta
ins some notable outbreakers—not just tent caterpillars of several kinds but also gypsy moths, tussock moths, larch budmoths, and others. Those are exceptions, though, to the general rule even for lepidopterans. Among all the forest-dwelling species of butterfly and moth, about 98 percent maintain relatively stable populations at low density through time; no more than 2 percent ever experience outbreaks. What makes a species of insect—or of mammal, or of microbe—capable of the outbreak phenomenon? That’s a complicated question that the experts are still trying to answer.

  An entomologist named Alan A. Berryman addressed it some years ago in a paper titled “The Theory and Classification of Outbreaks.” He began with basics: “From the ecological point of view an outbreak can be defined as an explosive increase in the abundance of a particular species that occurs over a relatively short period of time.” Then, in the same bland tone, he noted: “From this perspective, the most serious outbreak on the planet earth is that of the species Homo sapiens.” Berryman was alluding, of course, to the rate and the magnitude of human population growth, especially within the last couple centuries. He knew he was being provocative.

  But the numbers support him. At the time Berryman wrote, in 1987, the world’s human population stood at 5 billion. We had multiplied by a factor of about 333 since the invention of agriculture. We had increased by a factor of 14 since just after the Black Death, by a factor of 5 since the birth of Charles Darwin, and by doubling within the lifetime of Alan Berryman himself. That growth curve, on a coordinate graph, looks like the southwest face of El Capitan. Another way to comprehend it is this: From the time of our beginning as a species (about 200,000 years ago) until the year 1804, human population rose to a billion; between 1804 and 1927, it rose by another billion; we reached 3 billion in 1960; and each net addition of a billion people, since then, has taken only about thirteen years. In October 2011, we came to the 7-billion mark and flashed past like it was a “Welcome to Kansas” sign on the highway. That amounts to a lot of people, and certainly qualifies as an “explosive” increase within Berryman’s “relatively short period of time.” The rate of growth has declined within recent decades, true, but it’s still above 1 percent, meaning that we’re adding about 70 million people yearly.

  So we’re unique in the history of mammals. We’re unique in the history of vertebrates. The fossil record shows that no other species of large-bodied beast—above the size of an ant, say, or of an Antarctic krill—has ever achieved anything like such abundance as the abundance of humans on Earth right now. Our total weight amounts to about 750 billion pounds. Ants of all species add up to a greater total mass, krill do too, but not many other groups of organisms. And we are just one species of mammal, not a group. We’re big: big in body size, big in numbers, and big in collective weight. We’re so big, in fact, that the eminent biologist (and ant expert) Edward O. Wilson felt compelled to do some knowledgeable noodling on the matter. Wilson came up with this: “When Homo sapiens passed the six-billion mark we had already exceeded by perhaps as much as 100 times the biomass of any large animal species that ever existed on the land.”

  Wilson meant wild animals. He omitted consideration of livestock, such as the domestic cow (Bos taurus), of which the present global population is about 1.3 billion. We are therefore only five times as numerous as our cattle (and probably less massive in total, since they’re each considerably bigger than a human). But of course they wouldn’t exist in such excess without us. A trillion pounds of cows, fattening in feedlots and grazing on landscapes that formerly supported wild herbivores, are just another form of human impact. They’re a proxy measure of our appetites, and we are hungry. We are prodigious, we are unprecedented. We are phenomenal. No other primate has ever weighed upon the planet to anything like this degree. In ecological terms, we are almost paradoxical: large-bodied and long-lived but grotesquely abundant. We are an outbreak.

  111

  And here’s the thing about outbreaks: They end. In some cases they end after many years, in other cases they end rather soon. In some cases they end gradually, in other cases they end with a crash. In certain cases, even, they end and recur and end again, as though following a regular schedule. Populations of tent caterpillars and several other kinds of forest lepidopterans seem to rise steeply and fall sharply on a cycle of anywhere from five to eleven years. A population of tent caterpillars in British Columbia, for instance, has shown a cycle like that dating back to 1936. The crash endings are especially dramatic and for a long while they seemed mysterious. What could account for such sudden and recurrent collapses? One possible factor is infectious disease. It turns out that viruses, in particular, play that role among outbreak populations of forest insects.

  Back in 1993, when the caterpillars hit my town, I got interested in this subject and did some research. It seemed peculiar to me that a critter like the forest tent caterpillar, with a very limited repertoire of behavior, a fixed set of adaptive tactics, should multiply egregiously during one or two summers and then virtually disappear by summer three. The environment hadn’t changed drastically, yet the success of one species within that environment had. Why? Variations in weather didn’t explain it. Exhaustion of food supplies didn’t explain it. I called the county extension service and pestered a fellow there with questions. “I don’t think anyone can say why you have the boom and bust,” he told me. “It just happens.”

  Because that reply wasn’t satisfactory or convincing, I started reading the entomological literature. Among the experts in the field was one Judith H. Myers, a professor at the University of British Columbia, who had published several papers on tent caterpillars and an overview of insect population outbreaks. Myers offered a solution to the mystery. Although population levels are influenced by many factors, she wrote, the cyclical pattern “seems to imply a dominant force that should be easy to identify and quantify. That driving force, however, has proved surprisingly elusive.” But now ecologists had a suspect, she reported. Myers described something called nuclear polyhedrosis viruses, known collectively as NPVs, which “may be the long-sought driving force of population cycles in forest Lepidoptera.” Field studies had revealed that NPVs achieve their own outbreaks within outbreaking populations of forest lepidopterans, killing off the insects like the blackest of Black Deaths.

  For years I didn’t think much about this. The outbreak of tent caterpillars in my town ended quietly but quickly, back in 1993, with no sign of the hairy larvae the following summer. That was a long time ago. But the event came back to mind, during my work on this book, as I sat in the auditorium at a scientific conference on the ecology and evolution of infectious diseases. We were gathered in Athens, Georgia. The agenda was peppered with presentations on zoonoses, to be given by some of the frontline researchers and brainiest theorists in the field, and that’s what had attracted me. There would be a talk on Hendra virus and how it emerges from flying foxes; there would be a talk on the spillover dynamics of monkeypox; there would be at least four talks on influenza. But the second morning of the conference began with something different. I sat down politely, and then found myself mesmerized by a smart, puckish fellow named Greg Dwyer, a mathematical ecologist from the University of Chicago, who paced back and forth, speaking quickly, without notes, about population outbreaks and disease among insects.

  “You’ve probably never heard of nucleopolyhedroviruses,” Dwyer said to us. The name had changed slightly since 1993 but, thanks to the tent caterpillar episode, and to Judith H. Myers, I had. Dwyer described the devastating effect of NPVs on outbreak populations of forest lepidopterans. He spoke particularly about the gypsy moth (Lymantria dispar), another little brown creature, whose outbreaks and crashes he had studied for twenty years. He said that gypsy moth larvae essentially “melt” when infected by NPV. I wasn’t taking copious notes, but I did write the word “melt” on my yellow pad. I also wrote, quoting him: “Epizootics tend to occur in very dense populations.” After a few other general comments, Greg Dwyer went on to di
scuss some mathematical models. At the coffee break, I buttonholed him and asked if we could talk sometime about the fate of moths and the prospect of human pandemic disease. He said sure.

  112

  Two years passed, but then schedules came into alignment and I called on Greg Dwyer at the University of Chicago. His office, on the ground floor of a biology building just off East 57th Street, was cheerily decorated with the usual posters and cartoons and, along the left wall, a long whiteboard. Dwyer was fifty at the time and seemed young, like an amiable grad student whose beard had gone gray. He wore round tortoiseshell glasses and a black T-shirt printed with a grotesquely complex integral equation. Above and below the equation, the shirt asked in large letters: WHAT PART OF [this gobbledygook] DON’T YOU UNDERSTAND? The shirt was a metajoke, he explained to me. The gobbledygook was one of Maxwell’s equations; the joke part, of course, was that no average person would understand the thing at all; the meta part, I think, was that Maxwell’s equations are famous but so notoriously abstruse that even a mathematician might not recognize this one. Get it?

  We seated ourselves on opposite sides of his desk but then, as soon as the conversation got rolling, Dwyer jumped up and began drawing on the whiteboard. So I stood too, as though being closer to his scribblings would help me comprehend them. He drew a set of coordinate axes, one axis for the number of gypsy moth eggs in a forest, the other axis for time, and explained how scientists measure an outbreak. Between outbreaks, the gypsy moth is so scarce it’s undetectable. During an outbreak, in contrast, you find thousands of egg masses per acre. With about 250 eggs in each egg mass, that yields a lot of moths. He drew a graph depicting the rise and fall of a gypsy moth population over successive years. It looked like a Chinese dragon, the line of its back arching way up and then dropping way down, way up again, then again way down. He drew a sketch of NPV particles and described how they package themselves for protection against sunlight and other environmental stresses. Each packet is a solid lump of protein, polyhedral in shape (hence the name) and containing dozens of virions embedded like bits of cherry in a fruitcake. Dwyer drew more graphs and, while drawing, explained to me how this nefarious virus works.