The Viral Storm

by Nathan Wolfe

  We tend to think of events like sex or childbirth as intimate, and they certainly bring together individuals in ways that normal interactions cannot. But from the perspective of a microbe, hunting and butchering represent the ultimate intimacy, a connection between one species and all of the various tissues of another, along with the particular microbes that inhabit each one of them.

  The butchering in our own kitchen bears little resemblance to the hunting and butchering that our common ancestor would have engaged in eight million years ago. While these first hunting events are now lost, they probably held much in common with the chimpanzees I saw sharing their red colobus meal in Kibale—the dominant male holding down the animal with one hand and using its other hand and teeth to pull apart the skin of the gut while seeking a preferred organ. I remember seeing the chimpanzee holding the organ in its hand, its fur slicked down with blood, and thinking to myself that it would be nearly impossible to imagine a better situation for the movement of a new microbe from one species to the next.

  While we still hunt and butcher, the ways that we do so and the methods we use to prepare meat differ radically from the methods of the past. The early ancestors of humans and chimpanzees lacked the ability to cook, they lacked tools for butchering, and they certainly lacked dental hygiene! Whether through a wound from a broken monkey bone, an open sore in the mouth, or a cut on the arm, the microbes of hunted animals infected these animals in ways that had not occurred prior to the advent of hunting. Hunting fundamentally changed how they were exposed to the microbes in their worlds, many of which had remained relatively isolated in the animals that shared the forests with them. As much as hunting represented a milestone for our eight-million-year-old ancestors, it had equal importance for the world of our microbes.

  Chimpanzee eating its hunted prey, a red colobus monkey. (Nathan Wolfe)

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  There are many methods for comparing animals within an ecosystem. We can chart the diversity of foods they consume, the diversity of habitats they utilize, the range of space that they cover within an average year. We can also consider them based on the diversity of microbes they possess, what I call their microbial repertoire. Each species has a particular microbial repertoire. It includes viruses, bacteria, parasites—all of the various microbes that can call that species home. And while no single animal within a species will likely have all of the various pieces of the microbial repertoire at any one time, it acts as a conceptual tool for measuring that species’ microbial diversity—the range of microbes that infect it.

  Species vary considerably in terms of their microbial repertoires. And hunting and butchering do not provide the only avenue for microbes to jump from one species to the next. Species that don’t hunt or butcher still have regular exposure to the microbes of other species. Blood-feeding insects provide an important route for microbes to move around. Mosquitoes, for example, often feed on a range of different animals, in effect acting as physical carriers on which microbes can hitch a ride to move from species to species within ecosystems. Similarly, contact with waste from other animals, either through direct contact or indirect contact through water, also provides critical connections in the networks that permit microbes to negotiate the otherwise largely separated worlds of different host species.

  Nevertheless, mosquitoes and water provide narrow paths from one host to the next. Mosquitoes, for example, are not syringes. They are fully functional animals that have their own immune systems, and even those microbes that can manage to evade the mosquitoes’ defenses will be limited to those in the blood. Similarly, water generally passes on those microbes that live in the digestive tract. Hunting and butchering, in contrast, provide superhighways connecting a hunting species directly with the microbes in every tissue of their prey.

  When our ancestors began to hunt and butcher animals, they put themselves at the center of the vast web of microbes living in the full range of tissues of their various prey animals. Whether in the form of a virus in the brain of a bat, a parasite in the liver of a rodent, or a bacterium living on the skin of a primate, the microbial worlds of these various species suddenly converged on the common ancestor, changing for them (and ultimately us) the range of microbes that they would carry.

  The impact that the advent of hunting had on the microbial repertoires of the common ancestor and its descendants would continue to play itself out over millions of years. As the lineage of the common ancestor diverged, multiple species (chimpanzees, bonobos, and humans) would emerge, each with the capacity to hunt. These species would go on to accumulate their own sets of novel microbes from the animals on which they preyed. At times, these species would collide when their habitats overlapped, allowing them to exchange microbes, with serious consequences for both species.

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  Because humans are focused largely on our own health, we often forget that cross-species transmission is not a one-way street. This was brought home for me in vivid detail during my time working with chimpanzees in the Kibale Forest in Uganda. On one afternoon, people from a local village came into our research camp asking for assistance. The distraught villagers explained that a chimpanzee had grabbed an infant child and severely bitten his brother, who had tried to protect it. The infant had not been seen again and was presumably eaten by the chimpanzee. Upon a visit to the village, an eyewitness confirmed the young boy’s story. The nasty bite wound on his upper arm was a reminder that would stay with him forever.

  The events made me think more carefully about chimpanzee predation, and a subsequent analysis with my colleagues revealed that the event was not unique. Reports from as early as the 1960s had documented similar events. Although it was not a common activity, chimpanzees had hunted humans, usually infants, especially those who were left close to the edge of the forest while their mothers worked on their farms. While disturbing, the idea that chimpanzees occasionally hunt people should not surprise us. From the perspective of a chimpanzee, a red colobus monkey, a forest antelope, and a human infant would all represent logical potential prey. In the same way, humans, while occasionally observing food taboos, hunt opportunistically and generally consume the full variety of local animals in their environment. Whether a closely related ape or a more distantly related antelope, they all present opportunities for vital calories, and both chimpanzees and humans exploit every one of them.

  The fact that chimpanzees hunt humans and humans hunt chimpanzees would come to have significance for the two species’ microbial repertoires. In the years that followed the advent of hunting by the common ancestor, these two closely related but ecologically distinct species would each accumulate substantive microbial diversity through hunting and other routes. And then, critically, from time to time they would exchange microbes. We’ll explore the range of implications that this exchange has in the coming chapters.

  As the human lineage broke off and diverged, going through a near extinction event, but then coming back full force with agriculture, animal domestication, and, later, global travel and practices such as blood transfusions, the connections with our ape cousins would continue to have importance for our microbial repertoires in sometimes surprising ways. As we’ll explore, the role of this close connection continues now with chimpanzees and other apes acting as the missing piece of the puzzle in some of our most important diseases. Two close primate relatives—chimpanzees that live and hunt diverse animal species in central Africa, and humans with rapidly expanding territory and globally interconnected relationships—would prove to be an important combination. A recipe for pandemics.

  3

  THE GREAT MICROBE BOTTLENECK

  We knew it was somewhere nearby, but the area didn’t seem quite right. Driving through miles of seemingly endless savanna in Uganda’s Queen Elizabeth National Park, we saw only a dozen or so trees, and not the right kind. These were short, solitary, wide-crowned trees, completely engulfed by the never-ending dry grass. Small groups of zebra and the unique Ugandan Kob antelope dotted the landsc
ape. But this did not seem like a a place for a rain forest—certainly not for chimpanzees. It was too open, too dry, too much of a, well, savanna. Yet as we came to the peak of an embankment, there it was—a massive gaping vein of green in the sea of yellow grass. The Kyambura Gorge.

  The gorge, while not the only one of its kind, is unusual. Cut through the center by a river flowing from a rain forest some hundred or so miles away, it provides a unique microclimate—a well-hydrated strip in an otherwise dry landscape. Along that strip, rain forest trees and the animals that depend upon them slowly migrated downstream. This occurred over tens and hundreds of thousands of years, but now when you sit in the middle of the usually dry savanna habitat in Queen Elizabeth Park, you see a thriving rain forest, complete with chimpanzees. Effectively, you see the finger of a faraway forest snaking its way into the savanna.

  Kyambura Gorge. (© Alice Mutasa)

  This gorge provides a unique interface. For contemporary researchers, it provides a fairly easy way to follow chimpanzees. By simply driving along the unobstructed sides of the gorge, we can follow the calls of chimpanzees and then dip down into the gorge to locate them. This is a far cry from the much more challenging work of chasing them through the forest on foot. For the chimpanzees, the gorge provides something much more meaningful. Instead of the few grassland edges in a normal chimpanzee habitat, river gorges like Kyambura provide miles and miles of savanna border along a relatively typical chimpanzee habitat, allowing chimpanzees to explore and utilize the grassland much more than their rain forest contemporaries. And use it they do. Some populations enjoy spending a good deal of time in the savanna, even hunting savanna animals.

  Sometime after the split between the lineages that would lead to chimpanzees and bonobos on the one hand and humans on the other, our ancestors embarked upon a trajectory that would include a series of changes moving them away from the lifestyle of the common ancestor. Sitting on the edge of Kyambura Gorge, it is hard not to consider one of the most dramatic of these changes: the shift from being a primarily forest-based animal to an animal with the capacity to live in and utilize grassland. While the order of the events remains somewhat opaque, at some point our ancestors began to make forays into the savanna. This move would ultimately alter their microbial repertoire and their future.

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  As contemporary humans, we normally think of chimpanzees and bonobos, if we think of them at all, as a side-note species. They are interesting animals, certainly, with much to teach us about our history, yet they hover somewhere near the brink of extinction and live in marginal forest habitats, certainly not species that could compete with humans. Shocking as it may seem, this was not always the case. If we could see the world millions of years ago, say around that time that human lineages and chimpanzee/bonobo lineages diverged, it would be very different. Six million years ago, it was an ape’s world.

  In our modern world with over six billion humans and only an estimated one to two hundred thousand chimpanzees and ten thousand bonobos, humans have reached every point on Earth, and all of the wild chimpanzees and bonobos remain confined to central Africa. We have to stretch our brains to imagine a world in which we were the minority. Yet for some periods prior to the advent of agriculture around ten thousand years ago, that was exactly the world in which our ancestors lived.

  Chimpanzees and bonobos are not fossils. Contemporary species, whether chimpanzees, bonobos, or humans, have all changed since this aforementioned ancient time. Nevertheless, around six million years ago when our own ancestors took their first tentative steps toward becoming human, they would have seemed much closer to our chimpanzee and bonobo relatives than to ourselves. Our relatives at that time were almost certainly covered with thick hair. When on the ground, they primarily moved around by walking on all fours but really spent the majority of their time in the trees. They hunted—collective and strategic hunting as we’ve seen. But they didn’t cook their meat, didn’t use tools that couldn’t be simply modified from tree branches, and kept largely to the forest.

  As our own lineage changed and began to display some of the features that we equate with humans, the world was a different place. The use of grasslands was perhaps not completely foreign, and even today some small groups of chimpanzees utilize mosaic environments with forest as well as grasslands, like the Kyambura chimpanzees, yet they did not likely make long journeys into these habitats. At that early time, the individuals that spent time in grasslands were the odd ones.

  Often when groups of individuals veer into new areas, they do so to escape intense competition, and as our own ancestors moved to savanna habitats, they probably did so less to break new ground than simply to find somewhere they could exist with fewer rivals. Such habitat moves often led to marked inefficiencies, and when our early ancestors relocated, they probably experienced profound disadvantages. Being unsuited, at least at first, to function in grasslands, our early ancestors suffered a number of consequences that likely included smaller population sizes. Or near extinction.

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  Determining historic population sizes, particularly prior to periods in which we have written records, is fraught with difficulty. But studies suggest that our ancestors’ population densities were sometimes very low, with lower numbers than those of current gorilla and chimpanzee populations, and at least once teetered on the brink of extinction. Our ancestors would have been an endangered species. We believe this to be the case because our genes maintain some of these records, and by comparing the genetic information among contemporary human populations with that of our close ape relatives, we can tease out inklings of relevant information.

  The information revealed is striking. Analyses of the human mitochondrial genome, a region of genetic information that passes only from mother to daughter, as well as studies of mobile genetic elements that accumulate in regions of the genome in a clocklike way provide clues to our historic population size and suggest it was much smaller than we might expect.

  Our preagricultural ancestors likely lived in small groups, which is not necessarily surprising. Most of our evolutionary history as primates was spent in forested environments. And while exact timelines for the main events remain unknown, moving from forested environments to savanna habitats, shifting from largely fixed territories to a more nomadic lifestyle, and adapting to the various new conditions imposed by these changes must have been traumatic. An apt comparison might be the idea of contemporary humans living on Mars. The generations of our ancestral populations that confronted the savanna frontier probably did so at some cost. But our interest in small population sizes here is less about the consequences for humans and more about the consequences for microbes.

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  Low population densities, such as those exhibited by our ancestors, have a marked impact on the transmission of infectious agents. Infections need to spread. If population sizes are low, it is much harder for this to happen. The scientific term for substantially reduced population sizes is population bottlenecks, and when population bottlenecks occur, species should be expected to lose their microbial diversity.

  Microbes can be largely divided into two different groups, acute and chronic, and each group is impaired in small host populations. In the case of acute agents (like measles, poliovirus, and smallpox) infections are brief and lead either to death or immunity from future infections: they kill you or make you stronger. Acute microbes require relatively large populations; otherwise, they will simply burn through the susceptible individuals, leaving only the immune or the dead. In either case, they go extinct. If there’s no one left to infect, that’s the end of the line for a microbe.

  Chronic agents (like HIV and hepatitis C virus), unlike acute agents, do not lead to long-lasting immunity in their hosts. They hang on to their hosts, at times holding on for a host’s entire lifetime. These agents have a better capacity than acute agents to survive in small populations. Yet during severe population bottlenecks, even chronic agents suffer from higher rates of
extinction. Just like the probability that a particular gene will be lost during a population bottleneck (a phenomenon that results in inbreeding in small populations), the probability that a chronic agent will be lost should also be expected to increase when populations are small. If someone dies, and they are the last individual carrying the microbe, then the microbe dies.

  The role of population bottlenecks in diminishing microbial repertoires, what I call microbial cleansing, likely had an effect when the population sizes of our ancient ancestors crashed, resulting in populations with a lower diversity of microbial agents. In some cases, microbial cleansing would have led to situations where agents present for millions of years in our ancestors disappeared. Agents that had accumulated following the advent of hunting and other agents that were simply part of our heritage just vanished. While we don’t normally think of microbes as a part of our family heritage, in many ways that’s exactly what happens—they pass down to us from our ancestors, but from time to time they die out. And while microbial cleansing sounds like a very good thing, it would prove to be a double-edged sword.

  A population bottleneck: a diverse population (top) is greatly diminished by a near-extinction event (middle), resulting in a more homogenous population (bottom). (Dusty Deyo)

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  Sometime following the split between the chimpanzee/bonobo lineage and our own, another important change occurred in our ancestors that would have dramatic consequences for our microbial repertoires: they learned to cook. Not Michelin three-star cuisine, of course, but cooking nonetheless: using heat to prepare food. Exactly when our ancestors harnessed the power of fire remains a mystery. Presumably, fire first provided warmth and security from predators and competitors. Yet it appears to have quickly become a profound way of altering food. Richard Wrangham, my mentor from Harvard, discusses cooking and its consequences in depth in his well-researched book Catching Fire: How Cooking Made Us Human. Among other things, he analyzes in detail cooking’s origins.