Evolutionary success is all about looking out for number one - or so most biologists would tell you. The genes that do the best job of passing themselves along to the next generation, whether by brute selfishness or canny cooperation, are the ones that flourish - a view most memorably championed by Richard Dawkins more than 30 years ago in his bestselling book The Selfish Gene.

Almost everyone agrees that the gene’s-eye view works perfectly well most of the time. “It’s dominated the field, and dominated for a long time,” says Michael Ruse, a philosopher of science at Florida State University in Tallahassee. Indeed, many biologists think the selfish-gene concept can explain all the intricacies thrown up by evolution, and not just the obviously selfish ones.

However, the consensus is that evolution never favours what might be called “selfless” genes - that is, adaptations that benefit a group of organisms or the species as a whole. An example would be a gene that restricts how many offspring a predator has, to avoid wiping out its prey. Such a gene should always lose out to selfish genes that maximise reproduction, the thinking goes, even if reproducing without restraint threatens the survival of the whole species.

, and on several fronts. The least controversial of these is the notion that entire species themselves can have traits that, over geological time, make them more likely than others to escape extinction and branch off new daughter species. This can lead to evolutionary change that could not be predicted from individual adaptations alone.

Just how important is species selection, though? “How frequent is it, and how often does it operate counter to individual selection? We don’t have a good sense of that yet, because so few people are testing at multiple levels,” says Jablonski.

However, species selection could yet turn out to play a stronger role in other situations. We shouldn’t expect it to be important all the time, Simpson notes. After all, even gene or individual-level selection - which everyone agrees is a potent force - often produces little net change for long periods of time.

Certainly, group selection can be a powerful force in artificial situations. Indeed, crop breeders rely on it, often without realising they are doing so. Choosing the most vigorous individual plants produces hyperaggressive plants that, when grown together in a field, interfere with each other so much that yields go down. Instead, crop breeders choose plants that get along well, by growing them in test plots and breeding from the plots that yield best - in effect, practising group selection.

Similarly, a host of lab experiments over the past several decades have shown that group selection can lead to evolutionary change. These experiments are done in controlled situations, though. In the real world of nature, group selection may not have such an easy time, because cooperative groups are vulnerable to takeover by cheaters. These selfish invaders - a fast-growing wheat plant, for example - pay none of the costs of cooperation, yet reap all the benefits of being in a cooperative group. In the lab, or in breeders’ test plots, researchers can parry this influx of selfish genes. Since nature lacks such oversight, most biologists doubt group selection can be important. “The interesting question,” says Dawkins, “is whether any adaptation of a wild animal or plant is interpretable as group selection. I don’t think it is.”

That may be changing, though, as fresh ideas emerge that give group selection some theoretical traction. In particular, David Sloan Wilson of Binghamton University in New York state has shown that cheaters will not prosper if groups frequently break up and reform again with new members. With each fresh start, the groups that happen to have the least cheaters thrive while those with lots of cheaters perish.

Microbial biofilms are one of the best test cases for this hypothesis. Biofilms are colonies of bacteria living within a matrix of slime that they secrete. They enrich the slime with molecules that help them extract nutrients, such as iron, from the environment. “Single bacteria produce these compounds that scavenge the iron, but once this molecule is produced, it’s a common good, and you can get cheats arising,” says Alexandra Penn, an evolutionary biologist at the University of Southampton in the UK.

Ecosystem selection

Penn’s models suggest that not only should there be group selection, but that evolution can make the conditions needed for group selection more likely in the future. In other words, if cooperative biofilms do better than selfish ones, the result will be slime that persists just long enough to favour group selection. Penn is beginning experiments to see whether the bacteria’s slime does indeed evolve towards the consistency her work suggests is ideal for group selection.

Microcosms

This idea remains anathema to most mainstream evolutionary biologists. According to the conventional view, individual species in an ecosystem should be the equivalent of cancerous cells in a body, perhaps cooperating with some other species but growing as aggressively as possible heedless of the cost to the whole ecosystem.

Finding out whether there is ecosystem selection or not isn’t easy. A decade ago, for example, Sloan Wilson and his colleagues grew microcosms containing hundreds of species of soil microbes. With each “generation” they tested the microcosms to see which could support the greatest plant biomass, and used the soil from the winning microcosm to found new microcosms. After 16 generations, the selected soil ecosystems could support three times the biomass of similar, unselected soils. Since they were selecting for a property of the whole ecosystem, not of any individual microbial species, what was happening was ecosystem selection, they argued.

But the experiment had a key shortcoming. “There was no way they could rule out the possibility that they just got an ecosystem that happened to have a good batch of individual species in it,” says Hywel Williams, an evolutionary modeller at the University of East Anglia, UK. So Williams set to work to repeat the experiment using a detailed computer simulation instead of actual organisms. In Williams’s model, digital organisms take in nutrients, metabolise them and excrete wastes, altering their environment. They grow, reproduce and evolve - with the key difference that, with the click of a computer mouse, Williams can turn off individual selection to see whether a separate, ecosystem-level evolution is also occurring.

Context is all

Sure enough, when Williams and his colleague Timothy Lenton simulated the effects of selecting ecosystems that approached some ecosystem-level target (such as acidity levels), they found that ecosystem-level selection best explained their results. “We found that you couldn’t decompose the response we observed at the community level to a lower-level response. There was no single species that could do the job on its own,” says Williams.

Penn, too, has seen evidence of ecosystem-level selection in experiments using soil microcosms, and she expects to see something similar within her microbial biofilms, where multiple species may work together to produce an environment that maximises their collective survival and reproduction. “It’s meaningless to say you’ve just got individual selection in that case,” she says. “If you looked at each species individually, you couldn’t predict what they’d be doing. You have to look at them in the context of the ecosystem.”

If ecosystem-level selection is the norm, it could prompt a major shake-up in our view of the microbial world and, by extension, the macroscopic world, too. “It’s only in the last 5 or 10 years that people realised that the majority of bacteria live in multispecies collectives,” says Penn. “Bacteria are driving the basic processes of the biosphere, so if their evolution is in this higher-level context, it’s going to be very different to the way we’ve thought about it previously, and their responses to climate change could be very different than we would expect from thinking about them individually.”

It is still too early to know whether group, species and ecosystem-level selection are major evolutionary forces or merely minor curiosities - baroque ornaments on the central edifice of individual or gene-level selection. But the dominance of the “selfish gene” in evolutionary thought is facing its strongest challenge in many years.

The selfish network?

The gene’s-eye view of evolution puts individual genes centre stage, but some critics charge that this misses the real picture. Genes rarely act alone. Instead, they operate as part of networks of interacting genes, in which multiple genes affect each trait and each gene affects multiple traits.

What’s more, these networks usually have enough redundancy that deleting any one gene has little if any impact on an animal’s form or function. If so, it is the network - not the individual gene - that is selected, says Eva Jablonka, an evolutionary biologist at Tel-Aviv University in Israel.

Gene’s-eye proponents, such as Richard Dawkins of the University of Oxford, counter that only by looking at the fitness of the genes themselves, averaged over all their possible contexts, can one really understand evolution. “The other genes in the pool are part of the environment in exactly the same way as predators and parasites and everything else,” Dawkins says.

Others think the relentless focus on the gene misses the point for another reason. “They’re saying life is all about the transmission of instructions, not about what’s done with those instructions,” says Niles Eldredge, a palaeontologist at the American Museum of Natural History in New York. “And yet, it’s what’s done with the instructions that determines the fate of those instructions. If you just look at genes, you’re not going to see why evolution happens.” Evolutionary biologists should focus on the physical or behavioural traits being selected, Eldredge says, not the genes that underlie them.

The response of the Dawkins camp is that genes carry information in a stable form from one generation to the next, usually changing only slowly, while individuals flicker in and out of existence. It therefore makes more sense to study genes - the replicators - rather than their temporary vehicles. Read more at www.newscientist.com