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IF YOU want to make steam rise from an evolutionary biologist’s ears, try suggesting that evolution might have a goal or purpose. The idea has been anathema for more than a century, ever since biologists rejected Jean-Baptiste Lamarck’s idea that giraffes that stretched to reach high branches could pass their long necks on to their offspring. Evolutionary change, we know, results from random mutation and natural selection, and any notion of purpose smacks of creationism and its close cousin, intelligent design. “That’s the third rail of evolutionary theory,” says Peter Corning – anyone who treads near it risks a severe shock to their reputation.

But Corning, director of the Institute for the Study of Complex Systems in Friday Harbor, Washington, is one of a handful of people who are tiptoeing, gingerly, into the danger zone by . And they are not talking about a few rare curiosities. If they are right, this evolutionary steering has played a crucial role in the history of life on Earth. It may even have been significant in the evolution of humans.

It is important to note at the outset what these radicals are not saying. They are not saying that evolution has an intrinsic tendency towards larger size, greater complexity or increasing intelligence. They are not saying that organisms can order up the mutations they need whenever they need them – although individuals might be able to roll the genetic dice more often when environments are dire and they need a bit of luck (see “Gambling on evolution“). And they are not saying that organisms can pass on the habits of a lifetime to their offspring in a Lamarckian fashion.

What they are saying is something subtler. Over their lifetimes, living things make all sorts of adjustments to their physical being – what biologists call the phenotype, as opposed to the genetic make-up, or genotype – to get along better in the environment they find themselves in. They grow differently based on how they use their bodies, they turn certain genes on and others off, they learn new behaviours, and so on.

None of these changes count as evolution, because they don’t directly change the organism’s genetic make-up. But they do shape the way natural selection acts on these genes, and in that way they push evolution in a different direction. In effect, the genes, which we have always thought of as occupying the driver’s seat, have slid over to let the phenotype take the wheel. When the phenotype changes for some purpose, the genes that enhance that response might come along for the ride.

“Over their lifetimes, living things make all sorts of adjustments to their physical being”

One process that allows phenotypes to change in potentially useful directions is an individual’s development. “The magic of development is that even in unusual circumstances it responds in a useful way,” says Richard Palmer at the University of Alberta in Edmonton, Canada. A classic example is the unfortunate goat studied by Dutch anatomist E. J. Slijper in the 1940s. Born with paralysed front legs, it learned to walk on its two hind legs. When Slijper dissected the goat after its death, he found that the bones in its legs, chest and spine were a different shape to those in other goats. Its leg muscles also attached to its leg bones in a way that more closely resembled those of bipedal animals such as humans. Similarly, crabs that feed on hard-shelled prey develop thicker, more powerful crushing claws than those that feed only on soft-bodied prey, says Palmer.

So far, so uncontentious. But the question is, when phenotypes go down a particular path, do the genes follow? A few studies suggest that they do. Take sticklebacks. and his colleagues found that the fish, which usually migrate between fresh and salt water in western Canada, develop two different body shapes depending on what they eat: plankton feeders are large-eyed and slim-bodied with an upturned jaw, while bottom feeders are heavier with smaller eyes and a horizontal jaw. However, some sticklebacks have more recently evolved to live permanently in lakes. These also specialise in one food source or the other, but here genetics largely determine the body shape of the fish, not the food source itself. In other words, the genes have taken control of what was once a purely developmental effect.

Similarly, in some social insects, the female that happens to be the biggest and most dominant becomes the queen. But in most highly evolved species, all females have the genes to be queen, although these are only activated in those fed special food. This suggests that, over the course of evolution, the development of queens has come to be guided by a more elaborate genetic programme, says Mary Jane West-Eberhard, a Smithsonian Tropical Research Institute scientist at the University of Costa Rica near San José.

The notion that evolution might work this way is actually an old one, dating back more than a century to biologist J. M. Baldwin, but only recently has this “Baldwin effect” begun to enter the mainstream. Palmer emphasises that the underlying mutations still happen by chance: “Mutation is random, but development is not.” Changes to the phenotype that emerge from developmental processes are very often beneficial to the organism, he says, at which point natural selection can pick out those that have genetic variants favouring those useful responses.

Random handed?

Examples like these are interesting, but is this phenotype-led evolution common enough to be a major player in how life evolves? That is a much harder question. Perhaps the best evidence to date comes from the evolution of left-right asymmetries. These are not uncommon in nature – think of crabs with one claw larger than the other, flounder with both eyes on one side of the head, or the coiling of a snail shell. Palmer combed through the literature to find groups of species with asymmetries, and then examined their family trees to infer how they had originated. He found 35 cases in which asymmetries appeared to arise from genetic mutations favouring one side or the other, and almost as many – 33 – in which the initial asymmetry probably arose through some accident of behaviour or development (). What’s more, in as many as 28 other cases, an initially random handedness was later converted into a genetically fixed handedness – strong evidence that the genes were often following development.

A handful of studies of other traits also support the notion of genes as evolutionary followers rather than leaders. “If we can come up with this many examples from the literature, maybe it’s something that needs to be taken more seriously,” says Carl Schlichting at the University of Connecticut in Storrs.

In many of these cases, the developmental changes are triggered by behavioural choices – food preferences, hand preferences and so on – that were made by individual organisms. Behaviour presents perhaps the clearest instance in which organisms put a purposeful spin on their interactions with their environment. Nowhere is this more apparent than in “niche construction“, in which organisms engineer their environments in what can be profound ways. A beaver’s dam, for example, converts meadow into wetland, creating the deep pools to which the beaver is adapted, says Kevin Laland at the University of St Andrews, UK. In effect, the beavers are making the environment adapt to them, instead of the other way round.

“Beavers are making the environment adapt to them, instead of the other way round”

“This is a crucial point,” says Laland. “We look outside and see this beautiful fit between organisms and their environment. We generally interpret that as the product of an endless series of deaths, which has gradually fashioned the population to become well suited to the environment. But there are actually two processes. Yes, there’s natural selection, but there’s also this process of niche construction whereby organisms can modify environmental states, often in ways that are beneficial to the organisms. So that match is a two-way street, rather than a one-way street.”

Of course, the most sophisticated form of niche construction is human culture. The idea that culture has affected our genes is well established. The switch to farming 10,000 years ago, for example, triggered the evolution of extra genes for enzymes used in starch digestion, and other genetic changes that allow some human groups to digest milk sugars as adults. More speculatively, the much earlier invention of cooking may have made the diet of early humans more nutritious, thus providing enough energy for the evolution of our large, energy-expensive brains.

Genomic studies show that natural selection has been unusually active on a wide range of genes since the dawn of human agriculture, says Peter Richerson at the University of California, Davis. We don’t know what most of these genes do, he says, but clearly culture, which is unquestionably a goal-directed activity, has had a huge effect on our genomes.

Follow my leader

“People often analogise the gene-culture coevolution process in humans to a process of self-domestication,” says Richerson. “I don’t think it’s controversial to say that when humans select wheat plants for higher yield and cattle for docility, that this is a sort of purposive selection of domesticates. If humans are auto-domesticated, then you could say that we’re acting purposefully on our genome.”

Plausible as all these arguments may be, most evolutionary thinkers aren’t yet persuaded that genes might often be followers, rather than leaders, in evolution. Indeed, many define evolution as changes in gene frequency over time, which necessarily puts genes in the driver’s seat. Particularly influential in shaping this view is Richard Dawkins’s 1976 book The Selfish Gene, which allows no room for behaviour or development to lead the evolutionary dance. “Which elements,” Dawkins writes, “have the property that variations in them are replicated, with the type of fidelity that potentially carries them through an indefinitely large number of evolutionary generations? Genes certainly meet the criterion. If anything else does, let’s hear it.” Dawkins brushed off 91av‘s request for comment with a curt “I have nothing to add”. But proponents of a more nuanced view of evolution do. “Evolution is phenotypic change underlain by gene frequency change,” says West-Eberhard. “But it has become distorted to say that evolution is genetic change. If you start saying that, you lose the phenotype and you start to think of selection as just about gene frequency. That’s what happened to a whole generation, really.”

“If humans are self-domesticated, then you could say that we are acting purposefully on our genome”

It may sound like a simple difference in emphasis, but it matters. If genes do often follow the evolutionary direction pioneered by phenotypes, this has important implications for the evolutionary process. Flexibility in development and behaviour can help organisms adapt to new environments even when they lack the genetic raw material, says Richerson. For example, birds with larger brains – and hence more flexible behaviour – are more likely to establish themselves when introduced into novel environments. “Big-brained birds like crows and parrots are easy to introduce; a few escaped pets and they’re on their way,” he says.

Something similar may underlie the bursts of diversification that often happen when a species colonises a new habitat. One study of fish and amphibians, for example, . Just imagine if the first finch to reach the Galapagos Islands had lacked the behavioural ability to try new foods, says Corning. Darwin would have had to look elsewhere for evidence of evolution.

That could be the tip of a very big evolutionary iceberg. “I think learning has been enormously important in evolution,” says Eva Jablonka of Tel Aviv University in Israel. “Once learning evolved, it is the driving force in animal evolution.” In fact, Jablonka thinks the evolution of associative learning may have been what sparked the Cambrian explosion, the relatively sudden burst of diversification that produced almost all of today’s animal phyla about 550 million years ago. If she is right, then we owe almost everything – from the diversity of animal life to human culture – to the ability of organisms to direct evolution towards useful ends.

This article appeared in print under the headline “Life’s purpose”