The Viral Storm

by Nathan Wolfe

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  The close relationships we have with dogs, whether as companions, work animals, dinner guests, or a source of food, should not surprise us. Dogs play a special role in human history. If we were to compile the “greatest hits” of human evolution, hunting and cooking would certainly make the cut. Language and the capacity to walk on two feet would also be on the list. But central among our species’ critical historical events is domestication—and dogs were the first in a long line of plants and animals that our ancestors tamed.

  The capacity to domesticate plants and animals underlies much of what we now think of as being human. To imagine a world without domestication, we’d have to spend time with one of the few dozen human populations on the planet that still practice hunting and gathering lifestyles, groups like the Baka and Bakoli, the so-called pygmies, living in central Africa that I have worked with for years, or the Aché that live in South America. For these groups of people, there is no bread, no rice, no cheese. There is no agriculture, and therefore the many rituals of our planet’s major traditions, including the harvest and planting pilgrimages and their associated festivals, are entirely absent—no holidays such as Ramadan, Easter, or Thanksgiving. There is no wool, no cotton, only textiles made from wild tree bark or grasses and the skins from hunted animals.

  These hunter-gatherer populations have complex histories, and many of them lived at some point with some form of agriculture before returning to a foraging lifestyle. Yet they provide us with interesting clues on what the lives of our ancestors looked like before the advent of widespread domestication.1 Among the traits hunter-gatherer populations share are small population sizes and a nomadic lifestyle. As we’ll see, these traits have an important impact on keeping the microbial repertoires of these populations at low levels.

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  The first human foray into domestication came with modification of wolves into the canines we know today. Archaeological and DNA evidence suggests that populations in the Middle East and east Asia began domesticating gray wolves as early as thirty thousand years ago, turning them into guard dogs and work animals as well as using them for food and fur. The early history of dog domestication is still unclear. One hypothesis is that wolves followed humans, scavenging off of their kills, and over time became dependent on humans, a dependency that set the stage for their later domestication. But no matter how it began, by fourteen thousand years ago dogs played an integral role in human life and culture. In some archaeological sites in Israel, humans and dogs were even buried together. These early dogs would have resembled modern-day basenjis, the silent hunting dogs preferred by the central African hunters with whom I work.

  Occurring around twelve thousand years before we would domesticate anything else, the domestication of the dog was an early precursor to what would follow. Around ten to twelve thousand years ago, a domestication revolution occurred in earnest, starting with sheep and rye and then followed by a diverse group of other plants and animals.

  Female Basenji dog. (Dave King / Getty Images)

  The consequences and opportunities of the domestication revolution were profound. Prior to domestication, human populations were limited by the food available in wild environments. Wild animals migrate, which forced our ancestors, who were dependent on the hunting of these wild animals, to do the same. The wild fruits and other plant foods present in the local habitat were spread out, which again forced seasonal movement. Wild environments, with a few minor exceptions,2 lacked the capacity to sustain large populations of people. As a consequence, human population sizes were small, probably numbering no more than fifty to a hundred people in a group, and mobile.

  Human population through history. (Dusty Deyo)

  As domestication truly kicked in around five to ten thousand years ago, this would all change. With a combination of domesticated plants and animals, humans gained the capacity to have sustained sources of calories year-round. Agriculture (i.e., the domestication of plants) made it possible for human populations to stay in one place and avoid the constant movement that characterizes hunting-and-gathering populations as well as populations with only domesticated animals, which need to move in order to find feed for their herds. A sedentary lifestyle and the capacity for food surplus radically increased the potential for populations to grow, leading to the first real towns and cities. The particular combination of larger population sizes, sedentary groups of humans, and the growing populations of domestic animals would play a central role in transforming the relationship between humans and microbes. But humans aren’t the only animals that tame the wild.

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  Despite conventional wisdom, the capacity for domestication is not unique to humans. The most striking example of domestication in the animal kingdom comes not from primates, dolphins, or elephants—in fact, not from a vertebrate species of any type—but from ants. Far from simple-minded insects, ants are part of unique and complex colonies, each of which is perhaps better imagined not as a group of individual ants but rather as a collective ant “superorganism.”3

  Leaf-cutter ant colonies exist in most tropical American habitats. Known to schoolchildren worldwide for their incredible strength, the workers march through the jungle carrying pieces of green leaves many times their own size back to the nest. Yet the leaf-cutter’s strength is not its most interesting feature. This amazing group of ants has mastered the art of domestication. Rather than eat those massive leaves, the workers chew them up into a fertilizer. The colony uses the fertilizer in order to support their gardens—for leaf-cutter ants, made up of the Atta and Acromyrmex groups, cultivate a fungus-based crop and have spent millions of years living off it. These ants are farmers.

  Leafcutter ants in a fungus garden, Belize. (Mark Moffett / Getty Images)

  Domestication of fungus has helped leaf-cutter ants become one of the most successful species on our planet. Mature leaf-cutter colonies, measuring fifteen meters across and five meters deep, can house upward of eight million ants. The massive underground colonies are sedentary, sometimes lasting for more than twenty years in the same location.

  These remarkable ants have attracted a number of scientists, including a Canadian researcher named Cameron Currie. Dr. Currie has used molecular tools to examine the genetics of the ants, their fungus, and the other members of this incredible community. His research has shown the evolutionary links between the ants and their fungus crop. The colonies and their crop species have lived together for tens of millions of years, a much more mature farmer-crop relationship than that seen in humans.

  Like human farmers, the ants have agricultural pests, including a specialized fungal parasite that spoils the farms. Dr. Currie has shown that not only have the ants and their crops lived together for millennia; the parasitic fungus has been along for the ride since the beginning. Another amazing twist to this elegant system is that, like human farmers, the ants utilize a pesticide. They cultivate a species of bacteria that produces fungicidal chemicals that help the ants control their vermin. Some people think of ants as pests, but these ants have their own pest problems.

  Humans began domesticating other species merely thousands of years ago, rather than millions, as with the leaf-cutters. Like the ants, we’ve found that one of the consequences of high crop densities is parasites. The fungus species that the ants cultivate almost certainly had pests tens of millions of years ago, before they were cultivated by the leaf-cutters. But when the leaf-cutters accumulated the fungus and added fertilizer, it allowed more fungus to live closer together than resources would have permitted without active farming. Cultivation leads to concentrated populations, and concentrated populations have higher burdens of parasites, whether fungus or virus.

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  While the leaf-cutters focus exclusively on farming fungus, humans have taken agriculture and livestock to entirely new levels. Rather than cultivate a species or two over the course of a few millennia—lightning speed in evolutionary terms—humans domesticated a vast range of plan
t and animal species.

  We take it for granted, but the diversity of living things that our species cultivates boggles the mind. In an average day, we might wake up in sheets (cotton) and wool blankets (sheep); put on leather shoes (cow) and perhaps a cashmere sweater (goat); eat a breakfast of eggs (chicken) and bacon (pig); bid farewell to our pets (dog, cat) on the way to work; for lunch we might eat a salad (lettuce, celery, beets, cucumber, garbanzo beans, sunflower seeds) with dressing (oil from olives); for a snack we might eat a fruit salad (pineapple, peaches, cherries, passionfruit) or mixed nuts (cashews, almonds, peanuts, actually a legume); for dinner a caprese salad (tomato, buffalo mozzarella) and pasta (wheat) with peas and smoked farmed salmon with fresh basil (all domesticated). It would be an uncommon day for many of us not to interact with at least three domesticated animals and a dozen or so domesticated plants. We are truly masters of domestication.

  Consumption of wild foods, the source of calories for virtually all other organisms on our planet, now represents an almost quaint luxury for most humans. My friends Noele and Giovanni make a delicious wild asparagus pate from plants gathered in woods outside their small hillside village near Reggio, Italy. But using wild vegetables is now the exception rather than the rule. Wild salmon costs significantly more than farmed salmon in the vast majority of the world. Eating wild venison, something my friends Mimi and Chris like to do each year in their Massachusetts cabin, represents a challenging “return to nature” rather than a regular source of calories.

  The transition from a species primarily dependent on wild sources of nutrients to a species that cultivates most of its food means that we don’t need to depend on the fluctuating food availability in uncultivated habitats. It also allows for the concentration of these activities, with a few individuals focused on developing food while the rest of us have time to pursue other objectives, like, say, virology. We are freed from the daily foraging required of our ancestors before domestication. For our purposes here, it also radically changed the way that we related to the microbes in our world.

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  In the field sites where I work throughout the world, my collaborators and I work closely with hunters and monitor for new microbes that cross into them as they catch, prepare, and consume wild animals. Yet the hunters are not our only focus. Among the things we study in rural villages are the domestic animals—the dogs, goats, pigs, and other species that surround these people. Each animal, wild and domestic, has their own microbial repertoire, and when concentrated on a farm or in a house or herd, these microbes thrive.

  Domestic animals have contributed novel microbes to humans in different ways. Since these species each had their own predomestication microbial repertoires, the initial close contact of farming led to an early exchange of their microbes to humans. My colleague Jared Diamond has provided detailed evidence for this exchange and its consequences for human history in his excellent book Guns, Germs, and Steel. Among other things, Jared showed that the preponderance of domestic animals in temperate regions contributed to a higher diversity of microbes among temperate populations. For example, measles descends from rinderpest, a virus of cows that entered into humans, a domestication-associated virus that continues to plague us.

  Humans have close interactions with domesticated animals, whether for companionship, protection, or food. These interactions reach fascinating extremes. In Papua New Guinea, women in some ethnic groups actually suckle their pigs, providing human breast milk to ensure the survival of these valuable animals. This level of close connection has obvious implications for the movement of infectious agents.

  Of the microbes that originated in our domesticated animals, many entered into humans thousands of years ago, at or near the time that we first domesticated them. Acquiring the microbes that belonged to our domestic animals played an important role in enhancing the microbial repertoire of our ancestors during the climax of domestication five to ten thousand years ago. Over time, this has changed. In the case of dogs, for example, most of the microbes that they had to contribute to humanity have already crossed over. In some ways, the microbial repertoire of our species has merged with that of dogs and the other animals we’ve domesticated. Even without breastfeeding our domestic animals, we often cuddle with them for warmth or play. We almost always have closer connections to them than we would to wild animals.

  The historical “predomestication” dog microbes that had the potential to cross into humans have largely done so, and the human microbes that could survive in dogs have also crossed. The ones that haven’t crossed successfully likely don’t have the potential to, and while they may lead to occasional infections in one or two individuals, they won’t have the capacity to spread—the critical trait required for something to have true impact.

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  Over the thousands of years of interaction, we have reached a sort of microbial equilibrium with domestic animals. But this doesn’t mean that these animals don’t still contribute to our microbial repertoire; quite the contrary. Domestic animals continue to feed new microbes into the human species. These bugs derive not from the animals themselves, but from wild animal species that they are exposed to. Our domestic animals act as microbial bridges, permitting new agents from wild animals to make the jump into us.

  There are numerous examples of domestic animals bridging the microbial divide between humans and wild animals. Perhaps the best documented of these is the case of Nipah virus, a fascinating bug whose emergence has been studied in detail by my collaborators Peter Daszak and Hume Field and their colleagues. Through years of viral sleuthing, they have shown in exquisite detail exactly how the virus negotiates the complex world of humans and our farms.

  Nipah virus was first detected in Malaysia, in the village that gave it its name. This virus kills. Of the 257 cases of infection seen during 1999 in Malaysia and Singapore, 100 people died, a startlingly high mortality rate. Among the survivors, more than 50 percent were left with serious brain damage.

  The first clues to the origin of the virus were the patterns of human cases. The vast majority occurred among workers in piggeries. At first, the investigators thought the virus causing the illness was Japanese encephalitis virus, a mosquito-borne virus present throughout tropical Asia. Yet menacing and distinct symptoms led the investigating teams to determine that it must be a new and still unidentified agent.

  Early symptoms of Nipah virus include those common in viral infections—fever, decreased appetite, vomiting, and flu-like systems. But after three to four days, more serious nervous system manifestations appear. The exact impact that the virus has differs from person to person. Some individuals experience paralysis and coma, while others have hallucinations. One of the first documented patients reported seeing pigs running around his hospital bed.

  MRI scans show serious damage to patches of the brain, and the patients who die usually do so within a few days of the onset of brain damage. Among the individuals infected in Malaysia and Singapore in 1999, none appeared to seed additional human infections, yet cases in subsequent years in Bangladesh provide evidence that the virus has the potential to spread from human to human under at least some circumstances.

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  When scientists discover a new virus, a mad rush often ensues to identify the reservoir of the virus—the animal that maintains it. While certainly useful, the concept of a reservoir also has limitations. Scientists often see stark divisions between species. We neatly divide up the world of animals into families, genera, and species, but we often forget that these divisions are based on our own conventions. A taxonomist can clearly sort out the difference between a colobus monkey, a baboon, a chimpanzee, a gorilla, and a human, yet the traits that permit us to classify these animals as distinct are, as I’ve mentioned, often irrelevant for a microbe. From the perspective of a virus, if cells from distinct species share the appropriate receptors, and ecological connections provide the appropriate opportunities to make a jump, the fur of a baboon or the upright status o
f a human does not matter at all.

  Some viruses persist permanently and simultaneously in multiple hosts. Dengue virus, a viral infection originally called breakbone fever because of the intense pain it causes, appears largely in human cities. Yet dengue also lives in wild primates in tropical forests, where it is referred to as sylvatic dengue.4 Sylvatic dengue simultaneously infects multiple species of primates and does not discriminate. It has a wide host range.

  Among the numerous dry technical scientific papers that I digested as a doctoral student, few are indelibly etched on my brain. One that I remember in detail was a report describing experiments to determine the host range of sylvatic dengue.

  In the study, which used outdated methods now considered unethical, scientists put various species of primate into cages and used ropes to lift the cages high into the canopy where dengue’s forest mosquitoes feed. There they gathered samples of viruses to determine which species had the potential for infection. The study largely worked—except in one case where they brought the cage down only to find a massive python with a very badly distended abdomen. The large snake had entered the cage to consume the trapped and no doubt terrified monkey. Having miscalculated, the satiated snake could not squeeze through the bars to escape and found itself in the same trapped predicament as its monkey prey. Most likely the snake didn’t get infected with the virus; few viruses infect both reptiles and mammals. It did, however, make for a memorable photo in an otherwise dry technical journal.