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THERE鈥橲 no such thing as society. If you accept that evolution is all about
selfish genes, then the group has no role to play. Survival of the fittest means
survival of the fittest DNA. Which makes you and I mere vehicles in which our
genes are hitching a lift on the road to posterity. Or maybe not?

For forty years this rather bleak, reductionist view of life has reigned
supreme. Biologists ridiculed the idea that groups of organisms might gain a
survival advantage over other groups because they shared some beneficial trait.
Now that is changing. We are starting to understand that evolution happens on a
variety of levels. Natural selection may favour certain genes, but it can also
favour particular societies. Provided a group of individuals can cooperate
without any cheats trying to sneak an unfair advantage, then it may evolve as a
single entity.

In the most recent breakthrough, the high priest of group selection, David
Sloan Wilson from Binghamton University in New York state has found that even
groups made up of many different species can possess traits that are passed from
one generation to another. To some it looks like the biological equivalent of
quantum weirdness, but this is not just an academic oddity. Wilson鈥檚 finding
could allow biologists to create designer ecosystems that increase plant
productivity, change the pH of water or break down pollutants. In fact,
the implications of group selection apply to any situation where individuals
congregate鈥攆rom hens in the farmyard to parasites inside a human body.

Darwin first suggested group selection to explain why animals sometimes
behave in ways that reduce their reproductive success. In an extreme case, a
worker bee is unlikely to produce any offspring at all. How can this be, if
natural selection favours those individuals who send more of their progeny into
the next generation than their rivals? The objection applies to altruistic
behaviour of any kind, and Darwin addressed it in his discussion of the
evolution of humans, who show quite unnatural charitable tendencies. The anomaly
can be explained, he wrote, if you imagine natural selection operating among
groups of organisms, as well as among individuals. A group of people who are
kind and helpful to each other may not do so well individually, but as a team
they may do better than other groups of people, and so the tendency to work as a
team spreads through the population.

For almost a century, the group selection idea went unchallenged. But in the
1960s, some very influential biologists raised serious objections. Their main
argument was that within groups of generous individuals anyone who behaved
selfishly would have a huge advantage: so cheats and usurpers would always take
over the groups from the inside. Put another way, group selection is a very weak
force, compared with selection at the individual level. Over the next couple of
decades, other theories emerged to explain the evolution of altruistic
behaviour. They involved helping relatives, or helping only those who
reciprocate the favour, and they were backed up by mathematical models.
Mainstream biologists rejected group selection. It was swept under the carpet
and forgotten.

Natural progression

But the idea is experiencing a revival. In part this is due to the efforts of
mavericks like Wilson and his colleague Elliott Sober from the University of
Wisconsin at Madison, who never gave up on group selection. But, perhaps
surprisingly, the idea鈥檚 new respectability can also be traced to a shift in
thinking on the part of biologists who in the past have opposed group
selection.

The newly emerging view of evolution, proposed by John Maynard Smith from the
University of Sussex and E枚rs Szathm谩ry from the University of
Budapest, Hungary, describes the entire development of life as a series of major
transitions in which successively more complex levels of organisation have
become dominant. Each transition was a point when individual entities began
working together in a group and natural selection kicked in at a higher level.
When cells joined forces to make multicellular organisms, for example, cells
that cooperated fared better than cells that exploited the resources of the
group, because all the cells in an organism have a single, sealed fate. In this
new 鈥渕ultilevel selection鈥� view of life, group selection is a natural
progression.

Maynard Smith is convinced that group selection has been important at certain
points in the history of life, particularly between human groups in more recent
times. 鈥淭here is no doubt that we were way too hasty in trashing group
selection,鈥� agrees Joel Peck, also at the University of Sussex. 鈥淭he theoretical
models of the 60s and 70s were very over-simplified and should be taken with a
pinch of salt.鈥� Peck points out that along with the theoretical shift, a growing
number of experiments demonstrate that selection between groups does occur and
that it can be more powerful than selection between individuals.

In the early 1980s, for example, David Craig of the University of Illinois,
Chicago, conducted artificial evolution experiments with communities of flour
beetles living in glass vials. Each vial was allowed to produce a batch of young
beetles, some of which were selected and redistributed among new vials to form
the next generation. Craig tried selecting for and against the tendency to leave
the vial, which benefits the rest of the vial community because there is extra
space for those left behind.

When he selected only individual beetles that stayed in their vials, the
proportion of beetles leaving the vials did not change, even after 14
generations. But when he selected any group of beetles from populations where
there was a high proportion of emigrants, the number of beetles climbing out of
each vial doubled in 14 generations. 鈥淚n these experiments, individual selection
is weak, but group selection is very effective,鈥� says Peck. 鈥淲hich is exactly
the opposite of what we have all been taught.鈥�

Craig鈥檚 findings give clues about when and why group selection occurs. 鈥淭he
early models which rejected group selection assumed that altruistic traits were
controlled by a single gene, with two possible forms, that was directly
inherited from one generation to the next,鈥� says Peck. 鈥淓nvironmental variation
did not exist in those models.鈥� But group selection seems to be strong when a
trait is controlled not just by genes, but by interactions with the environment
and with other organisms. In genetic jargon, this is a trait with 鈥渓ow
丑别谤颈迟补产颈濒颈迟测鈥�.

The importance of interactions between individuals is shown by a group
selection experiment that could shake up the poultry industry. If you try to
improve the egg production of chickens kept in cages by selecting individual
birds that are the most fertile, you will find that productivity actually goes
down. This is because you are unwittingly selecting hens that are also
aggressive, who will snatch food from other birds in their cage. Put these birds
together and they will clash horribly, lowering overall fertility. In 1996,
William Muir and his team from Purdue University, Indiana, selected for high egg
production by picking out whole cages of birds that did well, rather than
selecting individual birds. They managed to increase annual egg production by
160 per cent, and the chickens lived so well together that they no longer had to
suffer the indignity of having their beaks cut off鈥攁 standard practice in
battery farming.

Group selection worked in this case because the trait 鈥渆gg production鈥� was
not just a property of the individual bird, but depended on the interaction of
many other birds in the group. Wilson and his research student William Swenson
wondered whether they could take this a step further. If selecting at group
level works on chickens, why shouldn鈥檛 it work on whole ecosystems, which have
many characteristics that are functions of the interactions between
organisms?

To test this possibility, Wilson and Swenson used soil鈥攁n ecosystem
made up of hundreds of thousands of individuals, from many different species of
fungi, bacteria and protozoa. They placed samples from a nearby forest in
several transparent containers and grew plants in these artificial microcosms.
After 35 days they selected those that had grown the most plant biomass, and
created a second generation of microcosms using soil from them. After 16
generations, the communities under selection were producing three times as much
plant biomass as other communities. The researchers conclude that some feature
of the soil ecosystem that enhances plant growth passes from one soil community
to another and is open to group selection.

鈥淧eople said it would never work,鈥� Wilson says. But it did. 鈥淭he concept of
selecting ecosystems without knowing about the actual organisms involved is
incomprehensible to some microbiologists, who think that the only good science
is to work with carefully isolated organisms . . .We would love to know what the
actual mechanism is. It鈥檚 likely to be something to do with interactions between
different organisms, but at the moment it鈥檚 a black box.鈥�

Wilson and Swenson have also found other ecosystems in which group selection
appears to work, for example the community of organisms living in pond water.
They found they could select for ecosystems that decreased the acidity of the
water. And in another experiment, they dramatically improved the ability of soil
ecosystems to digest a common chemical pollutant called 3-chloroaniline. This
method could have extensive commercial applications, especially because the
breakdown of contaminant chemicals often involves more than one type of
organism. 鈥淲hat we are doing here is developing designer ecosystems to do
certain tasks,鈥� says Wilson.

Inside evolution

If it is simple to do in the lab, then who鈥檚 to say that many features of
ecological communities have not evolved by group selection in nature? There are
countless examples of natural populations that are structured in discrete
groups鈥攆rom communities living on microscopic particles in the sea to
patchy populations of plants. The best example is parasites, which live in
groups of hundreds of thousands confined inside the bodies of their hosts.

鈥淢uch of the current interest in group selection is in parasitology,鈥� says
Peck. Disease organisms often evolve towards non-virulence, with each individual
parasite restraining its own reproduction so that the host can survive. This
means the rest of the parasite group can survive and disperse effectively.
鈥淓volution of non-virulence cannot be discussed without invoking group
selection,鈥� he adds.

Despite all the evidence, group selection remains unacceptable to some
biologists. Richard Dawkins, author of The Selfish Gene, has little
time for Wilson鈥檚 latest work. 鈥淭hey are interesting experiments, but have no
connection with group selection,鈥� he says. Dawkins accuses Wilson of trying to
resurrect an old biological heresy. 鈥淓normous credit would accrue to anybody who
could pull off the seemingly impossible and rehabilitate group selection,鈥� he
says. 鈥淏ut actually, such rehabilitation can鈥檛 be achieved, because the great
heresy really is wrong.鈥�

Dawkins argues that group selection is just a kind of kin selection, because
members of a group are always going to be related to one another, so helping
others means furthering the genes they have in common. 鈥淭here is only a revival
of group selection among people who have arbitrarily redefined kin selection as
group selection. It is particularly galling, since the term kin selection was
originally invented to distinguish it from group selection,鈥� he says. 鈥淟et鈥檚 get
on with pushing evolutionary theory ahead, without this tiresome,
time-consuming, backward-looking distraction.鈥�

Wilson responds that you could just as well say that kin selection is a type
of group selection. 鈥淚t is all a question of perspective,鈥� he comments, 鈥渁nd we
need different perspectives because they hold different insights.鈥�

While theoreticians bicker among themselves, the implications of group
selection may be extending far beyond the purely biological. Computer scientists
designing artificially intelligent software are showing an interest in these
techniques. 鈥淚mposing group selection on software agents or robots, by selecting
groups of components that work well for whatever reason, might just provide the
quantum jump that is needed in software development,鈥� says Peck. If he鈥檚 right,
group selection could be one of the most commercially successful ideas to have
emerged from biology for a long time.

NOMADIC hunter-gatherer groups such as the Inuit have a system of
egalitarianism in which everything is shared equally, and selfish behaviour is
severely punished. This extreme altruism is difficult to explain, because the
groups include unrelated individuals, and strict reciprocity does not operate.
But Chris Boehm, of the University of Southern California, Los Angeles, believes
he knows how the behaviour evolved.

鈥淏iologists agree that group selection is possible in theory, but it is such
a weak force that the existence of free riders would cancel it out,鈥� says Boehm.
Egalitarianism, he argues, has the effect of strengthening group selection and
weakening individual selection. It is all to do with variation鈥攖he raw
material on which evolution works. Within groups of egalitarian
hunter-gatherers, decisions are made by consensus, so variation within a group
is severely constrained. But variation between groups is enhanced because
different groups are likely to settle on different strategies. Survival of the
fittest becomes a competition among groups, favouring those that make the best
decisions about life-and-death matters, such as where to migrate each year.

Boehm believes, like Darwin before him, that morality evolved through group
selection because it acts as social glue sealing the combined fate of the group.
鈥淚f we assume that prehistoric humans were behaving in a similar way to modern
forager groups, then this process of selection between groups could have been
operating for 30 000 years,鈥� he says.

THE key to changing the level at which selection operates lies in suppressing
the interests of the individuals that make up the groups. 鈥淲hat intrigues me is
how this shift happens. What sort of conditions are required to make the
transition to a new level where freeloaders can no longer prosper?鈥� says Paul
Rainey, a geneticist at the University of Oxford.

Rainey works on bacterial cells that form floating microbial mats. Individual
bacterial cells in a mat produce a polymer that knits them together in a group.
The energetic cost of producing the polymer means that cells in the mats grow
more slowly than those living independent lives, but they benefit from floating
at the water surface, where the oxygen supply is good. 鈥淭his is a great system
to study group selection in, because there are well-defined costs and benefits
to the cooperation, and the groups are open to invasion by cheats,鈥� he says.

The cheats are cells that live in the mat, but don鈥檛 produce the polymer.
Rainey wonders whether he can impose an evolutionary transition on his microbial
mats, so that selection operating at the level of the group eliminates cheats by
favouring mats with only honest citizens. He is running test tube evolution
experiments in which mats with a low proportion of cheats are artificially
selected to form each successive generation. 鈥淭he results are looking good,鈥� he
says. 鈥淲e鈥檙e really interested in what mechanisms might spontaneously emerge to
counteract the invasion of cheats. At the moment we have no idea.鈥�