杏吧原创

HERE YOU ARE IN THE AMAZONIAN RAINFOREST of Peru. You鈥檝e braved the stifling
heat and humidity beneath the canopy to cordon off an area 100 metres square and
you begin to count the number of tree species within it. Your biological
training tells you that each species must occupy its own ecological niche, and
you know that the temperature is relatively constant, moisture is abundant, and
the type of soil varies little for thousands of square kilometres around your
test area. Vast diversity is the last thing you鈥檇 expect. But as you count, the
number rises past 100, then 200 and still rising. The final tally comes to about
600 mature trees from 300 different species.

How can this be? Why are there so many species and each one a rarity?
杏吧原创s have been trying to explain this diversity for nearly two centuries,
ever since Alexander von Humboldt ventured into the rainforest of the northeast
Amazon basin and astounded the world with accounts of the bewildering variety of
plants and animals he found. There has been no shortage of theories, though many
have been found wanting. Over the past two years, I have developed a theory that
seems to explain the patterns of growth and diversity found in rainforests. It
is based on a never-ending game of hide-and-seek played out between tree species
and the parasites and diseases that prey on them.

Three people have played a critical role in testing the theory, Stephen
Hubbell of Princeton University, Robin Foster of Chicago鈥檚 Field Museum, and
Richard Condit of the Smithsonian Tropical Research Station in Panama. They and
their many collaborators have spent the past 15 years studying growth within a
0.5 square kilometre plot of virgin Panamanian rainforest. It is the best place
in the world for testing theories of biodiversity.

Living laboratory

The plot is on an island in an artificial lake that forms part of the Panama
Canal, and has been isolated and protected since the birth of the canal in 1913.
Although not as diverse as the Amazonian rainforest, it contains 240 000 trees
of about 300 species. The positions and histories of all these trees are known:
how quickly they are growing and maturing, which trees have been born since
1981, and how many have died during that time.

Using this living laboratory, Hubbell and his colleagues have already tested
a number of ideas about rainforest biodiversity. One theory suggests that an
abundance of new ecological niches might appear briefly in the forest, for
example, when a large tree crashes down puncturing the forest canopy so that
sunlight floods in. Perhaps the variety of tree species that grow into the light
is greater than in the surrounding forest, so that little islands of
super-diversity are formed, each one feeding and replenishing the forest鈥檚
overall diversity. Hubbell ruled out this possibility, at least for the
Panamanian forest. The trees that grow into these shafts of light are no more
and no less diverse than the saplings waiting their turn in the surrounding
forest.

Another popular theory, proposed independently in the 1970s by Daniel Janzen,
working in Costa Rica, and Joseph Connell of the University of California, Santa
Barbara, explains diversity by focusing on the parasites and other pathogens
that exist in abundance in the rainforest. Suppose a species of tree is preyed
upon by a specific set of parasites which gather on and around it in large
numbers. Then seedlings of the same species that sprout near the parent tree
will often succumb to the pathogens, while those that grow some distance away
are more likely to survive. Experiments with seedlings deliberately planted at
various distances from large trees of the same species bear out the theory but
can this phenomenon account for overall rainforest diversity?

One prediction of the Janzen-Connell effect is that the trees of a given
species in the forest should be 鈥渙verdispersed鈥�: in other words spread out more
evenly than expected by chance. Unfortunately, the Panamanian rainforest data
strongly contradicts this prediction. All the species in the forest are clumped
rather than overdispersed. Any evidence of the Janzen-Connell effect is
weak.

My contribution to this debate came about quite accidentally. I have worked
in the laboratory rather than the field, investigating the causes of diversity
at the genetic level. A large number of genes are involved in resistance to the
many diseases and parasites that afflict almost all species of animals and
plants. Many of these genes come in a variety of forms, and evolve rapidly.
Recently, Douglas Green of the La Jolla Institute for Allergy and Immunology and
I developed a theory that we hoped might help to explain this genetic
diversity.

Thinly scattered

We began with the obvious. Much of the genetic diversity in humans has
evolved to protect us against the huge variety of pathogens that prey on us,
from viruses and bacteria to protozoa, worms and other parasites. This
inevitably means that some of us are more susceptible than others to a
particular disease. But we realised that genetic diversity can also protect this
susceptible group. If the people who are likely to catch a particular disease
are in a minority, then each of them will be surrounded by others who are more
resistant to the disorder. This makes life difficult for the pathogen causing
the disease, because the few susceptible hosts will be thinly scattered
throughout the resistant population. So many susceptible people might never come
in contact with the disease.

Of course, even faced with such adversity, the pathogens will rarely go
extinct. They have evolved many mechanisms to avoid extinction. But host
diversity will at least check their spread. This form of protection is akin to
that afforded by herd-immunity, a phenomenon known to farmers for decades. If
most of a herd is immunised against a disease, that disease can no longer spread
easily, and the few unimmunised animals are also protected.

But Doug and I went further by suggesting that herd-immunity might be caused
by genetic differences as well as by artificial immunisation. We modelled this
鈥済enetic herd-immunity鈥� on a computer, and showed that a genetically diverse
population of hosts ought to be able to keep many such diseases at bay
simultaneously. Whenever the number of hosts that are susceptible to one disease
grows too large, the pathogens that affect those hosts also begin to spread.
Eventually, their effect on survival or fertility drives down the number of the
susceptible hosts.

We realised that our model might also explain the extreme genetic diversity
that is often found in host populations. The more genetically diverse the hosts
are, the less likely it will be that any one type of pathogen can attack more
than a minority of its potential victims. Every pathogen will be confined to a
different, dispersed minority and so will be kept at low levels. So safety lies
in diversity, and evolution should increase this diversity.

Unfortunately the model is almost impossible to test. Establishing, say, a
genetically diverse colony of mice, subjecting them to a variety of diseases,
and then trying to guess which among thousands of genetic changes might have
determined their survival is simply too daunting a task to contemplate.

This is where matters stood in the summer of 1994 when I visited Peru to
research a book on the evolution of diseases. This beautiful country spans the
most ecologically diverse region in the world. The people too are diverse. In
the high Andes, they live on the edge of what is possible for human life, some
inhabit the lowland tropical rainforests, and still others occupy the dozens of
ecosystems that lie in between. Far too many of Peru鈥檚 people are afflicted by
diseases of poverty and of the tropics, and from a number of diseases unique to
the region. And they are surrounded by thousands of species of animals and
plants that are also plagued by disease.

The effect of non-human diseases became vividly apparent in parts of the
Peruvian rainforests that cover thousands of square kilometres to the east of
the Andes. I was struck not only by the teeming diversity, but also by the
pervasiveness of disease and death. After a mild windstorm had swept through the
forest, I spent hours crawling among the epiphyte-laden branches and shattered
tree trunks. Most were afflicted by a variety of fungi, blights, leaf-eating
insects, and bark beetles. What role did these hordes of parasites play? I began
to wonder whether a kind of herd-immunity might be operating here as well. But
in the rainforest it would operate at species level so it ought to be called
鈥渟pecies herd-immunity鈥�.

Species herd-immunity should allow many different species of tree鈥攅ach
individually rare鈥攖o coexist in the rainforest, protected by the diversity of
the tree species around them. And it should foster the evolution of greater and
greater diversity among the hosts. Trees in the forest should evolve to become
so diverse in their habits, morphology, and biochemistry that no one kind of
pathogen would be resourceful enough to attack them all. This host diversity
would keep many different kinds of pathogens at low numbers
simultaneously.

Back home I found that this idea had been largely anticipated in the 1960s by
Jan Gillett, an ecologist who had worked in tropical Africa, but he had been
unable to test it. So I contacted Steve Hubbell and Rick Condit, and together we
began to examine their Panamanian rainforest data to see if they showed any sign
of species herd-immunity.

We focused on the 84 commonest species in the plot. Then we divided the plot
into squares, called quadrats, and counted the number of trees of each species
in each one. We also noted the number that were born and died between 1982 and
1990. Species herd-immunity seemed to be operating in three quarters of species,
including all the most common ones. If there were few trees of a given species
in a quadrat, they tended to increase in numbers with time, while if there were
many, their numbers tended to decrease. This is what the species herd-immunity
model predicts. Pathogens should preferentially attack the most common species,
leaving rarer species free to increase鈥攗ntil they become common enough to
attract the attention of their pathogens.

One of the most important predictions of the model is that diversity should
benefit the whole ecosystem. If there is a great diversity of tree species in a
region of the rainforest, all their pathogens will be kept in check. But
diversity must be distinguished from sheer crowding, which would encourage the
spread of disease, just as infections spread easily in a crowded nursery school.
One measure of diversity that largely eliminates the complication of crowding is
a property called evenness. If a minority of the species in a quadrat are common
and the rest are rare, it is considered to have a low evenness. But if, in
another quadrat with the same number of species, all the species are equally
common, then that quadrat鈥檚 evenness is higher.

The species herd-immunity model predicts that diseases will tend to spread
more easily in quadrats with low evenness, because they have common species that
should fall prey to their pathogens. We found that this expectation was borne
out. In quadrats with low evenness deaths outstripped births, while in quadrats
with high evenness births outstripped deaths. But when crowding was considered
separately from evenness, the opposite was true. Diversity protects but crowding
does harm.

Evolutionary pressure

Pathogens are unlikely to be entirely responsible for safeguarding rainforest
diversity. But the Panamanian data have allowed us to rule out some alternative
possibilities. Suppose that trees of one species are more likely to survive and
reproduce when surrounded by trees of a second species than when encircled by
their own species. Perhaps the second species harbours a micro-organism in its
roots that benefits trees of the first species. This effect, too, if common,
would help to maintain diversity. But we found virtually no evidence for such
interactions.

On balance, it seems more and more probable that, as Jan Gillett suggested
decades ago, the evolutionary pressure of pathogens has had an enormous impact.
And while species herd-immunity is still just a hypothesis, it immediately
suggests exciting experiments. We now know which tree species in the Panamanian
rainforest are most density-dependent, and so most likely to yield interesting
results if their pathogens are studied. It should be possible to find out which
of their pathogens are most important, how specialised they are, and how they
keep in balance with their hosts. And what will happen if some of the pathogens
are removed from part of a rainforest? Will its diversity decline? It is ironic
that the diversity of a tropical ecosystem may depend on the presence of a
healthy crop of pathogens!

The evidence that supports species herd-immunity rests on the data set from
the Panamanian forest plot, which is the most extensive gathered from any
ecosystem. But other tropical ecosystems may be subject to different balances of
forces. Some rainforests, particularly in West Africa, for example, are made up
of surprisingly few species of mature tree. And we have no idea whether species
herd-immunity operates in regions far from the tropics. Does it operate in
temperate or even arctic ecosystems, where there are fewer host species and
presumably fewer pathogen species? What other processes might be operating? To
answer these questions we need data from different parts of the world that are
as extensive as the Panamanian data.

Greater understanding of the relationship between host and pathogen could
also help us to restore damaged ecosystems. The ecologist Thomas Lovejoy of the
Smithsonian Institution has followed the decline in diversity in a region of the
Brazilian rainforest partially cleared for agriculture. He has found that in
general the more fragmented the forest, the more rapidly species of animals and
plants are lost. It is usually assumed that most of these species are lost by
chance. But, if the zoo of pathogens plays an important role in maintaining
diversity, there is another grim possibility. Perhaps, as a few species of
plants race to recolonise cleared areas, the evenness of these zones is reduced
and the delicate balance between hosts and parasites is lost. Flare-ups of
disease could then help to drive host species to local extinction.

Testing the species herd-immunity model and other models for maintaining
diversity will add to our growing knowledge of the processes that have shaped
the Earth鈥檚 stunningly complex ecosystems. It may also help to give us the
knowledge we need to save them.