Spillover: Animal Infections and the Next Human Pandemic

Back in 2012, David Quammen predicted in his book Spillover that a novel coronavirus could prove to be the "Next Big One". This was not from prescience, but from listening to the right scientists.
Spillover: Animal Infections and the Next Human Pandemic
Adapted from Spillover: Animal Infections and the Next Human Pandemic. Copyright (c) 2012 by David Quammen. Used with permission of the publisher, W. W. Norton & Company, Inc. All rights reserved.
This excerpt is part of a series in which experts and thought leaders — from around the world and all parts of society — address for the OECD the COVID-19 crisis, discussing and developing solutions now and for the future. Aiming to foster the fruitful exchange of expertise and perspectives across fields to help us rise to this critical challenge, opinions expressed do not necessarily represent the views of the OECD.

Prior to the ongoing COVID-19 pandemic and emergence of the SARS-CoV-2 virus that caused it, I traveled the globe to better understand the devastating potential of animal infections transmissible to humans. Back in 2012, I predicted in my book Spillover that a novel coronavirus could prove to be the Next Big One. This was not from prescience, but from listening to the right scientists.

“The key is connectivity,’ Jon Epstein told me. He is a veterinary disease ecologist, employed at the time by an organisation called the Wildlife Trust (now, EcoHealth Alliance). I had accompanied him on a fieldtrip to southwestern Bangladesh in search of evidence of Nipah virus. “The key is to understand how animals and people are interconnected.” We were back at the hotel, showered and fed, after another full night of trapping, another fifteen bats sampled and released. You can’t look at a new bug or a reservoir host, he said, as though they exist in a vacuum. It’s a matter of contact with humans, interaction, opportunity. “Therein lies the risk of spillover.”

Repeatedly over the next half hour he returned to the word  “opportunity.” It kept knocking. “A lot of these viruses, a lot of these pathogens that come out of wildlife into domestic animals or people, have  existed in wild animals for a very long time,” he said. They don’t necessarily cause any disease. They have coevolved with their natural hosts over millions of years. They have reached some sort of accommodation, replicating slowly but steadily, passing unobtrusively through the host population, enjoying long-term security—and eschewing short-term success in the form of maximal replication within each host individual. It’s a strategy that works. But when we humans disturb the accommodation—when we encroach upon the host populations, hunting them for meat, dragging or pushing them out of their ecosystems, disrupting or destroying those ecosystems—our action increases the level of risk. “It increases the opportunity for these pathogens to jump from their natural host into a new host,” he said. The new host might be any animal […] but often it’s humans, because we are present so intrusively and abundantly. We offer a wealth of opportunity.

“Sometimes nothing happens,” Epstein said. A leap is made but the microbe remains benign in its new host, as it was in the old one (Simian foamy virus?). In other cases, the result is very severe disease for a limited number of people, after which the pathogen comes to a dead end (Hendra, Ebola). In still other cases, the pathogen achieves great and far-reaching success in its new host. It finds itself well enough suited to get a foothold; it makes itself still better suited by adapting. It evolves, it flourishes, it continues. The history of HIV is the story of a leaping virus that might have come to a dead end but didn’t. […]

“A lot of what determines whether a pathogen becomes successful in a new host, I think, is odds,” Epstein said. “Chance, to a large degree.” With their high rates of mutation, their high rates of replication, RNA viruses are very adaptable, he reminded me, and every spillover presents a new opportunity to adapt and take hold. We’ll probably never know how often that occurs—how many animal viruses spill into people inconspicuously. Many of those viruses cause no disease, or they cause a new disease that—in some parts of the world, because health care is  marginal—gets  mistaken  for  an  old  disease. “The point being,” he said, “that the more opportunity viruses have to jump hosts, the more opportunity they have to mutate when they encounter new immune systems.” Their mutations are random but frequent, combining nucleotides in myriad new ways. “And, sooner or later, one of these viruses has the right combination to adapt to its new host.”

This point about opportunity is a crucial idea, more subtle than it might seem. I had heard it from a few other disease scientists. It’s crucial because it captures the randomness of the whole situation, without which we might romanticize the phenomena of emerging diseases, deluding ourselves that these new viruses attack humans with some sort of purposefulness. (Loose talk about “the revenge of the rain forest” is one form of such romanticizing. That’s a nice metaphor, granted, but shouldn’t be taken too  seriously.)

Epstein was talking, in an understated way, about the two distinct but inter-connected dimensions of zoonotic transfer: ecology and evolution. Habitat disturbance, bushmeat hunting, the exposure of humans to unfamiliar viruses that lurk in animal hosts—that’s ecology. Those things happen between humans and other kinds of organism, and are viewed in the moment. Rates of replication and mutation of an RNA virus, differential success for different strains of the virus, adaptation of the virus to a new host—that’s evolution. It happens within a population of some organism, as the population responds to its environment over time.

Don’t imagine that these viruses have a deliberate strategy, he said. Don’t think that they bear some malign onus against humans. “It’s all about opportunity.” They don’t come after us. In one way or another, we go to them.

Among the most important things to remember about evolution—and about its primary mechanism, natural selection, as limned by Darwin and his successors—is that it doesn’t have purposes. It only has results. To believe otherwise is to embrace a teleological fallacy that carries emotive appeal but misleads. This is what Jon Epstein was getting at. Don’t imagine that these viruses have a deliberate strategy, he said. Don’t think that they bear some malign onus against humans. “It’s all about opportunity.” They don’t come after us. In one way or another, we go to them. […]

We should appreciate that these recent outbreaks of new zoonotic diseases, as well as the recurrence and spread of old ones, are part of larger pattern, and that humanity is responsible for generating that pattern. We should recognise that they reflect things that we’re doing, not just things that are happening to us. We should understand that, although some of the human-caused factors may seem virtually inexorable, others are within our control.

The experts have alerted us to these factors and it’s easy enough to make a list.

We have increased our population to the level of 7 billion [now almost eight billion, ugh, just a dozen years after I wrote that] and beyond. We are well on our way toward 9 billion before our growth trend is likely to  flatten.

We live at high densities in many cities. We have penetrated, and we continue to penetrate, the last great forests and other wild of the planet, disrupting the physical structures and the ecological communities of such places. We cut our way through the Congo. We cut our way through the  Amazon. We cut our way through Borneo. We cut our way through Madagascar. We cut our way  through New Guinea and northeastern Australia.

We shake the trees, figuratively and literally, and things fall out. We kill and butcher and eat many of the wild animals found  there. We settle in those places, creating villages, work camps, towns, extractive industries, new cities.

We bring in our domesticated animals, replacing the wild herbivores with livestock. We multiply our livestock as we’ve multiplied ourselves, operating huge factory-scale operations involving thousands of cattle, pigs, chickens, ducks, sheep, and goats, not to mention hundreds of bamboo rats and palm civets, all confined en masse within pens and corrals, under conditions that allow those domestics and semidomestics to acquire infectious pathogens from external sources (such as bats roosting over the  pig pens), to share those infections with one another, and to provide abundant opportunities for the pathogens to evolve new forms, some of which are capable of infecting a human as well as a cow or a duck. We treat many of those stock animals with prophylactic doses of antibiotics and other drugs, intended not to cure them but to foster their weight gain and maintain their health just sufficiently for  profitable sale and slaughter, and in doing that we encourage the evolution of resistant bacteria.

We export and import livestock across great distances and at high speeds. We export and import other live animals, especially primates, for medical research. We export and import wild animals as exotic pets. We export and import animal skins, contraband bushmeat, and plants, some of which carry secret microbial passengers.

We travel, moving between cities and continents even more quickly than our transported livestock. We stay in hotels where strangers sneeze and vomit. We eat in restaurants where the cook may have butchered a porcupine before working on our scallops. We visit monkey temples in Asia, live markets in India, picturesque villages in South America, dusty archeological sites in New Mexico, dairy towns in the Netherlands, bat caves in East Africa, racetracks in Australia—breathing the air, feeding the animals, touching things, shaking hands with the friendly locals—and  then we jump on our planes and fly home.

We get bitten by mosquitoes and ticks. We alter the global climate with our carbon emissions, which may in turn alter the latitudinal ranges within which those mosquitoes and ticks live. We provide an irresistible opportunity for enterprising microbes by the ubiquity and abundance of our human bodies.

That’s the salubrious thing about zoonotic diseases: They remind us, as St. Francis did, that we  humans are inseparable from the natural world. In fact, there is no “natural world,” it’s a bad and  artificial phrase. There is only the world.

Find out more about Spillover: Animal Infections and the Next Human Pandemic, by David Quammen (published in Sept. 2012, © W. W. Norton & Company)

And learn about the OECD's work in support of biodiversity and read the policy note Biodiversity and the economic response to COVID-19: Ensuring a green and resilient recovery
Find out more about the OECD's work in support of biodiversity and read the policy note Biodiversity and the economic response to COVID-19: Ensuring a green and resilient recovery

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