ONE WORLD
In 1998 scientists working independently in Australia and Central America an-
nounced that they were finding massive numbers of dead frogs in the forests
where they worked. The large-scale die-off was especially dramatic. Global amphib-
ian populations had been declining for some time, but these mounting frog deaths
occurred in pristine habitats—places far less likely to have been exposed to toxic
by-products of human cities or other man-made environmental threats. Field biolo-
gists and tourists alike witnessed the large numbers of dead frogs scattered about
the forest floor. This was rare indeed since scavengers quickly eat dead animals. To
see so many indicated that the predators already had their fill of free frogs and
these were the leftovers. In fact, it was just the tip of the iceberg. A massive and un-
precedented amphibian carnage was under way.
The expiring frogs all displayed similar and worrying symptoms. They became
lethargic, their skin sloughed off, and they often lost their ability to right them-
selves if turned over. In the months that followed the first announcements, a
number of possible explanations came forth—pollution, ultraviolet light, and dis-
ease among them. Yet the particular pattern of death was most consistent with an
infectious agent. Animal deaths spread in wavelike patterns from one location to
the next suggesting the spread of a microbe, a contagion sweeping through the
Central American and Australian frog world.
The solution to the mystery came in July 1998, when an international team of
scientists reported the source of the frog disease. The team found evidence that a
majority of the frog species succumbing to the die-offs were infected with a partic-
ular species of fungus. The fungus they identified was Batrachochytrium
dendrobatidis, known more simply as the chytrid fungus (pronounced KIT-rid).
They found evidence of chytrid, which had previously been seen exclusively in in-
sects and on decaying vegetation, on a number of dead frogs. Tellingly, when they
scraped the fungus from the dead and infected healthy laboratory tadpoles with it,
they were able to re-create the fatal symptoms. The fungus was to blame.
Since the 1998 report, this fungus is now documented on all continents that
have frog populations. It can survive at sea level but also wreaks havoc at altitudes
up to twenty thousand feet. And it’s a killer. In Latin America alone, chytrid fungus
has been linked to extinction in 30 of the 113 species of the strikingly beautiful
harlequin toads. Thirty species forever removed from the biological diversity of our
planet.
While the spread and devastation of chytrid has now been well documented,
much about it remains unknown. The large-scale declines in amphibian
populations predated the emergence of the fungus, so it is not the only problem
that is devastating global frog populations, but it’s definitely among them. Another
key factor is the steady decline in available frog habitat as the human footprint has
increased over the last hundred years.
The questions of where the fungus originated and how it spreads are largely
outstanding. Work done on archived specimens from South Africa shows that the
fungus has infected African frogs since at least the 1930s, decades before it hit any
other continent. This points to an African origin. Yet at some time, the fungus
spread and did so quite effectively. How did it manage to get so cosmopolitan so
quickly?
One possibility is the exportation of frogs. The researchers who discovered the
early evidence of chytrid in South Africa also noted that some of the species of the
frogs infected were commonly used in human pregnancy tests. When injected by
lab technicians with urine from pregnant women, African clawed frogs (Xenopus
laevis) ovulate—which made for an early, if significantly more cumbersome, ver-
sion of the common pregnancy dipsticks used today! Following the discovery of
this human pregnancy test in the early 1930s, thousands of these frogs were
transported internationally for this purpose. Perhaps they took chytrid fungus with
them.
But Xenopus was likely not alone in causing the global spread; since one stage of
the fungus’s life cycle actively spread in water, that was also a probable factor.
Human movement almost certainly played a role as well. Our shoes and boots are
at least partially to blame. This small fungus, wanted in the deaths of frogs world-
wide, hijacked us.
The chytrid fungus has resulted in global frog deaths and in some cases extinc-
tion of entire frog species, a tragic loss for wildlife on our planet. In a 2007 paper,
Lee Berger, one of the researchers who first identified the chytrid fungus, used lan-
guage uncommon in conservative scientific journal articles when he wrote, “The
impact of [chytrid fungus] on frogs is the most spectacular loss of vertebrate biodi-
versity due to disease in recorded history.”
What happened with the chytrid fungus also gives us important clues to a larger
phenomenon that affects much more than just amphibians. Over the past few hun-
dred years, humans have constructed a radically interconnected world—a world in
which frogs living in one place are shipped to locations where they’ve never
previously existed, and one where humans can literally have their boots in the mud
of Australia one day and in the rivers of the Amazon the next. This radically mobile
world gives infectious agents like chytrid a truly global stage on which to act. We
no longer live on a planet where pockets of life persist for centuries without contact
with others. We now live on a microbially unified planet. For better or worse, it’s
one world.
How did we get to this point? For the vast majority of our history as living organ-
isms on this planet, we had incredibly limited capacity to move. Many organisms
can move themselves over short distances. Single-celled organisms like bacteria
have small whiplike tails, or flagella, that allow them to move, but despite their
molecular-scale efficiency, flagella will never push their owners far. Plants and
fungi have the potential to move passively by creating seeds or spores blown by
the wind. They also have adopted methods that co-opt animals to help them move,
which explains the existence of fruit and the spores of fungi like chytrid. Never-
theless, precious few forms of terrestrial life regularly travel more than a few miles
in the course of their lives.
Among the wonderful exceptions to the largely static life on Earth is the coconut
palm. The seeds of the coconut palm (i.e., coconuts), like a number of other drift
seeds, evolved buoyancy and water resistance, permitting them to travel vast dis-
tances through ocean currents. Among animals, some species of bats and birds
are masters of space. The best example might be the Arctic tern, perhaps the most
mobile species on Earth outside of our own. The tern flies from its breeding
grounds in the Arctic to the Antarctic and then back again each and every year of its
life. A famous tern chick was tagged on the Farne Islands in the UK near the time it
was born in the summer of 1982. When it was found in Melbourne, Australia, in
October of the same year, it had managed a twelve-thousand-mile journey in the
first few months of life! It’s been estimated that these amazing birds, which can
live over twenty years, will travel about one and a half million miles in their life-
times. It would take a full-time commercial jet pilot, flying at the maximum FAA
permitted effort, nearly five years to cover the same distance.
Yet despite their wings, most bird and bat species actually live their lives quite
close to where they’re born. Only a few, like the Arctic tern, have evolved to
regularly move great distances. Highly mobile species, whether bird, bat, or
human, particularly the ones that live in large colonies, are of particular interest for
the maintenance and spread of microbes. Among primates, only humans have the
potential to move themselves great distances during a single lifetime, let alone in a
few days. That’s not to say that other primates simply stay put. Almost all species
of primates move every day in their search for food, and young adults routinely
move from one area to another before mating. Yet whether primate or bird, nothing
on the planet—certainly nothing outside of the sea—matches humans in our
capacity to move long distances quickly. The human potential to move, which now
includes traveling to the moon, is unique and unprecedented in the history of life
on our planet. But it comes with consequences.
Humans started globetrotting in earnest millions of years ago using our own two
feet. Bipedalism gave us an advantage over our ape cousins in terms of our capac-
ity to wander. And, as discussed in chapter 3, it had consequences for how we
interact with the microbes in our environment. Yet our capacity to negotiate the
globe in the amazing way we do now started with our use of boats.
The earliest clear archaeological evidence of boats dates to around ten thou-
sand years ago. Found in the Netherlands and France, these boats (which might be
better called rafts since they were made by binding logs together) were probably
used primarily in fresh water. The first evidence of sea-going boats comes from a
group of British and Kuwaiti archaeologists, who in 2002 reported finding a seven-
thousand-year-old vessel that undoubtedly was used at sea. The archaeologists
made their discovery at the Neolithic site of Subiya in Kuwait. Stored in the rem-
nants of a stone building, the boat consisted of reeds and tar. Most strikingly, the
bits of boat had barnacles attached to the tar, indicating that it was definitely used
in the sea.
Employing genetics and geography, we can get a much earlier estimate for the
first use of seafaring boats. The indigenous people of Australia and Papua New
Guinea provide perhaps the best case for this. By comparing the genes of the Aus-
tralasian people with other humans throughout the world, we can conclude that
people reached Australia at least fifty thousand years ago.
During this time, our planet was a relatively cold place—it was the peak of an
ice age. Since more of the Earth’s water was locked up in ice, the sea level was
lower, revealing pieces of land that connected what are currently islands. Many of
the islands in the Indonesian archipelago were joined by these so-called land
bridges.
Despite the land bridges that ice ages expose, we know that no one walked all
the way to Australia. In particular, the deep-water channel between Bali and Lom-
bok in present-day Indonesia, a channel around thirty-five kilometers long, would
have required boats to navigate. So we can infer that these early populations also
used at least some form of sea transport.
We know very little about these early Australian settlers, although we know that
they traveled at a time before animal domestication so certainly didn’t move with
animals in tow. Nevertheless, their movements impacted how they related with mi-
crobes. When they first crossed from Bali to Lombok, they encountered a com-
pletely novel set of animals.
The channel between Bali and Lombok lies squarely on Wallace’s Line, the fa-
mous geographic divide named after the nineteenth-century British biologist Alfred
Russel Wallace who, along with Charles Darwin, codiscovered natural selection.¹
While the distance between Bali and Lombok was no greater than that between
many of the waterways separating the hundreds of islands along the Indonesian
archipelago, Wallace noted that animal populations on either side of the channel
differed extensively. And while he didn’t have the precise models for ice age water
levels that we have today, he surmised that this biological divide existed because
Bali and Lombok were never connected by a land bridge, something we now know
to be true.
Like humans, other animals take advantage of land bridges, but unlike these
earlier settlers who had boats, the animal populations that couldn’t fly long dis-
tances were largely stuck on one or another side of this deep-water barrier. When
the first explorers left Asia for the Australasian continent, making the thirty-five-
kilo-meter hop from Bali to Lombok, they took a fairly short trip by boat but a huge
leap for primates. When they crossed this divide, these early explorers entered a
world that had never seen monkeys or apes before. They also encountered com-
pletely new microbes.
limited, since the small population sizes of the settlers wouldn’t have been able to
sustain many kinds of agents.
It’s hard to know exactly what the first trips across Wallace’s Line were like.
They may have been colonization events with small groups that were then com-
pletely cut off. Perhaps more likely they were short initial forays into new lands, fol-
lowed by the establishment of temporary outposts, much as we consider colo-
nizing the moon. The actual way in which the new lands were colonized would
have played an important role in determining the flow of microbes in either direc-
tion. And while these first Australasian humans almost certainly had some connec-
tions to the “mainlanders” they left behind on Bali, that contact may have been very
infrequent. Yet some new Australasian infections that had the potential for long-
lasting human infection could very well have made their first forays into human
populations on the Asian side of the divide.
The use of boats to visit new lands would continue with increasing frequency over
the forty or so thousand years following this first colonization of Australasia. We
have much better knowledge of what later trips were like and how they connected
microbially distant lands. Perhaps the peak of boating-based colonization before
modern times occurred among the Polynesian populations of the South Pacific.
Among these Polynesian journeys, probably the most incredible was the first
discovery of Hawaii, over two thousand years ago.² For the first lucky settlers, find-
ing this island would have been truly like finding a needle in a haystack. To give a
sense of scale, the largest island of the Hawaiian archipelago, also named Hawaii,
has a diameter of around a hundred miles. And the Southern Marquesas, whose
inhabitants were the most likely first colonizers of Hawaii, are some five thousand
miles away. To imagine what it would have been like to hit the mark, imagine we
blindfolded an Olympic archer, then spun him around and asked him to hit his tar-
get—the ratios are about the same. One can only imagine how many boats (and
their inhabitants) were lost before the fortunate finally made it.
On their long trips, the Polynesians probably lived largely on caught fish and
rainwater. Yet they traveled with a veritable biological menagerie. They brought
along sweet potatoes, breadfruit, bananas, sugarcane, and yams. They also traveled
with pigs, dogs, chickens, and probably (unintentionally) rats. Having all of these
domesticated species meant that the flotillas carried not only life support for the
Polynesian explorers, but also minirepositories of microbes, which would spread
and mix with local microbes in the places that they discovered.
The boat journeys of the Polynesians, as remarkable as they were for their time,
pale in comparison to the global shipping that emerged in the fifteenth and six-
teenth centuries. By the time Europeans reached the New World, in the late fif-
teenth century, thousands of massive sailing ships were plying the waters of the At-
lantic and Indian Oceans and the Mediterranean Sea, moving people, animals, and
goods back and forth between the countries of the Old World.
The impact of smallpox on New World populations is the most dramatic known
example of the way that the connections formed by shipping can influence the
spread of microbes. Some estimates suggest that as many as 90 percent of the
people living in the Aztec, Maya, and Inca civilizations were killed by smallpox
brought by boats during European colonization, a massive and devastating car-
nage. And smallpox was only one of many microbes that spread along the shipping
routes of this time.
Each of the major transportation advances would alter connectivity between
populations, and each would have their own impact on the spread of new mi-
crobes. The exclusivity of ships as a means for long-distance transport would not
hold out forever. The use of roads, rail, and air provided new connections and
routes for the movement of humans and animals as well as their microbes. For mi-
crobes, the transportation revolution was really a connectivity revolution. These
technologies created links that forever changed the nature of human infectious dis-
eases, including, critically, how efficiently they spread.
The use of roads of some sort or another is an ancient practice, far predating the
use of water as a medium for transportation. Chimpanzees and bonobos both cre-
ate and use forest trails to help them move through their territories. I learned this
firsthand while studying wild chimpanzees in the Kibale Forest National Park in
southwest Uganda. Richard Wrangham, the Harvard professor who introduced me
to this work, used these trails to help observe chimpanzees.
Wrangham had done his doctoral work at the Gombe Stream site in Tanzania
that Jane Goodall established. He’d critiqued some of the findings from Gombe
because the chimpanzees there were habituated by provisioning—to get the wild
chimpanzees comfortable with human researchers, the animals were fed large
amounts of banana and sugarcane. Wrangham felt that provisioning changed
some of the subtle chimpanzee behaviors, so when he started his own site in
Kibale, he habituated the animals the hard way—by having his teams follow them
until the apes effectively gave up and no longer ran away. He did this by essentially
enhancing and extending the natural pathways that they moved along.³
The art of actual road building began in earnest around five to six thousand
years ago when cultures throughout the Old World started using stone, logs, and
later brick to enable the movement of people, animals, and cargo. The first modern
roads followed in the late eighteenth and nineteenth centuries in France and the
United Kingdom. These roads used multiple layers, drainage, and eventually ce-
ment to make permanent structures permitting regular movement throughout the
year.
The rate at which modern roads have spread throughout the world has not been
consistent, of course. Some regions in Europe and North America have roads
reaching most human populations, while some regions where I work in central
Africa have virtually no road access. Clearly, as roads enter into new regions, they
bring both positive and negative effects. They are among the top priorities for many
rural communities since they provide access to markets and health care, but from
the perspective of global disease control, they are double-edged swords.
HIV is among the most notable example of the impact that road proliferation
has had on the movement of microbes. In a series of fascinating studies, the HIV
geneticist Francine McCutchan, whose lab I worked in at Walter Reed Army Insti-
tute of Research (WRAIR), and her colleagues at the Rakai and Mbeya sites in east
Africa have examined the role that roads have played in the spread of HIV, demon-
strating that proximity to roads increases a person’s risk of acquiring HIV. As peo-
ple have more access to roads, they have a higher chance of getting infected be-
cause roads spread people, and people spread HIV. Other than sex workers, the
highest occupational risk for acquiring HIV in sub-Saharan Africa is being a truck
driver. McCutchan and her colleagues have shown that the genetic complexity of
HIV is greater among individuals who have increased access to roads. Roads
provide the mechanism for different types of HIV to encounter one another, in a
single coinfected individual, and swap genetic information. But roads do more
than just help established viruses spread. Roads and other forms of transport can
also help to ignite pandemics.
One of the most stubbornly lingering public misconceptions is that we don’t know
how HIV originated. In fact, our understanding of the origins of HIV is more ad-
vanced than our understanding of the origins of probably any other major human
virus. As we saw in chapter 2, the pandemic form of HIV is a chimpanzee virus that
crossed into humans.⁴ There is no debate within the scientific community on this
point. The cumulative evidence with regard to how it originally entered into hu-
mans is also increasingly unequivocal. It was almost certainly through contact with
chimpanzee blood during the hunting and butchering of chimpanzees. We’ll delve
further into this in chapter 9 when we discuss the work my colleagues and I have
done with central African hunters.
Perhaps the only lingering debate about HIV origins is how it originally spread
from the first infected hunter and why it took so long for the medical community to
discover it. The earliest historical HIV samples date from 1959 and 1960, twenty
years before AIDS was even recognized as a disease. In an amazing piece of viral
detective work, evolutionary virologist Michael Worobey and his colleagues man-
aged to analyze a virus from a specimen of lymph node from a woman in
Leopoldville, Congo (now Kinshasa, DRC).
The lymph node had been embedded in wax for over forty-five years. By com-
paring the genetic sequence of the virus they found in the specimen with other
strains from humans and chimpanzees, they were able to attach rough dates for
the first ancestor of the human virus. While the genetic techniques they used can-
not pinpoint dates closer than a few decades, they concluded that the virus split
from the lineage sometime around 1900 and certainly before 1930. They also con-
cluded that by the time that the woman in Leopoldville became infected with HIV
in 1959 there was already a significant amount of genetic diversity of HIV in Kin-
shasa, suggesting that the epidemic had already established itself there.
The fact that HIV goes back to 1959, let alone 1900, provides some serious
challenges to the medical community. One of the central questions is this: if it was
in human populations in the early twentieth century and already constituted at least
a localized epidemic in Kinshasa by 1959, why did it take us until 1980 to identify
the epidemic? Another key question is what special conditions were present that
permitted the virus to start taking off in the middle of the twentieth century?
A number of changes occurred in francophone central Africa, the region where
HIV-1 originated, leading up to the period in the 1950s when those first precious
samples were taken. The anthropologist Jim Moore and his colleagues at the Univ-
ersity of California, San Diego, put together some of the key events in a 2000
paper, the majority of which focused on how easier means of travel influenced
virus proliferation. In 1892 steamship service began from Kinshasa to Kisangani in
the very heart of the central African forest. The steamship service connected pop-
ulations that had been largely separated, creating the potential for viruses that
previously might have gone extinct in local isolated populations to reach the grow-
ing urban centers. In addition, the French initiated the construction of railroads,
which, like shipping and road lines, connect populations. This produced another
mechanism for viruses to spread from remote regions to urban centers, effectively
providing a larger population size of hosts for a spreading virus.
In addition to the connectivity provided by new steam, rail, and road lines, the
construction of railroads and other large infrastructure projects led to cultural
changes that also had an important impact. Large groups of men were conscripted,
often forcefully, to build railroads. Moore and his colleagues note that the labor
camps were populated mostly by men, a condition that dramatically favors trans-
mission of sexually transmitted viruses like HIV. Together, the shipping and rail
routes and the factors surrounding their construction must have played a role in
the early transmission and spread of HIV.
As dramatic as the road, rail, and shipping revolutions were for the transmission of
microbes, an entirely new form of transport would add another layer of speed. On
December 17, 1903, in Kitty Hawk, North Carolina, a site chosen for its regular
breeze and soft sandy landing areas, the Wright Brothers made the first sustained,
controlled, and powered flight. Some fifty years later the first commercial jet flew
between London and Johannesburg. By the 1960s, the age of jet travel was here to
stay.
Airplanes link populations in an immediate way, which allows the transmission
of microbes to occur even more quickly. Microbes differ from each other in terms
of their latent period, the period of time between when an individual is exposed and
when they become infectious or capable of transmitting the agent to others.⁵ Al-
most no microbes that we know of have latent periods of less than a day or so, but
many have latent periods of a week or more. The immediacy of air travel means
that even microbes with very short latent periods can spread effectively. In con-
trast, if a person infected with an agent that had a very short latent period were to
board a ship, unless the ship had hundreds of individuals the virus could infect, it
would go extinct before the ship made land.
Commercial air flights alter in fundamental ways how epidemic disease spreads.
In a fascinating paper from 2006, my colleagues John Brownstein and Clark
Freifeld of Harvard, one of the new academic breed of digital epidemiologists, found
creative ways to use existing data to show just how much impact air travel has on
the spread of influenza. John and his colleagues analyzed seasonal influenza data
from 1996 to 2005 and compared it with patterns of air travel. They found that the
volume of domestic air travel predicts the rate of spread of influenza in the United
States. Interestingly, the November travel peak around Thanksgiving appears to be
of particular importance. International travel also plays a vital role. When the num-
ber of international travelers is lower, the peak of the influenza season comes
later—because when there are fewer travelers, it takes longer for the virus to
spread. Perhaps most strikingly the researchers were able to see the impact of the
terrorist attacks of September 2001 on influenza. The travel ban led to a delayed in-
fluenza season. The striking effect was not seen in France, which did not enact the
ban, providing an excellent control.
During the past few centuries the ease of movement has increased dramatically
throughout the world. The rail, road, sea, and air revolutions have all permitted hu-
mans and animals to move more quickly and efficiently both within continents as
well as between them. The transportation revolution has created interconnectivity
unprecedented in the history of life on our planet. It is estimated that we now have
over fifty thousand airports, twenty million miles of roads, seven hundred thou-
sand miles of train tracks, and hundreds of thousands of ships and boats in the
oceans at all times.
The connectivity revolution we’ve experienced has fundamentally changed the
ways that animal and human microbes move around our planet. It has radically in-
creased the speed at which microbes can travel. It has brought populations to-
gether, allowing agents that couldn’t previously sustain themselves with low popu-
lation numbers to flourish.
As we’ll see in chapter 8, it has also permitted completely novel diseases to
emerge and frightening animal viruses to extend their ranges. These technologies
have created a single interconnected world—a giant microbial mixing vessel for
infectious agents that previously stayed separate and stayed put. The new microbial
mixing vessel that our planet has become has forever altered the way in which we’ll
experience epidemics. It has truly helped usher us into the pandemic age.
