http://www.newscientist.com/channel/life/mg19926752.200-freedom-from-selection-lets-genes-get-creative.html

As if from nowhere?

What if nature’s most elaborate creations “just happened”?

Christine Kenneally is intrigued by anew twist to evolution.

Terry Deacon’s theory of “something for nothing” is challenging our ideas of how complex traits emerge.

●THE Bengalese finch is an aviary bird, bred over centuries for its attractive plumage. It comes in various combinations of white, black and brown. One particularly pretty version is silver. It is also prized for its gregarious and easy-going nature and its complex warbling song. Which is strange because the finch’s closest wild relative, the white-rumped munia has a simple, predictable song as well being incredibly shy and easily upset. How could the finch, bred for its colour, have evolved these other elaborate traits as well?

Solving the puzzle of the Bengalese finch promises to throw light on a much larger question in biology – how nature creates complex things. We tend to think of evolution as a brutal race and behavioural complexity as a brilliant strategy that is honed by the competition. On the track, runners try to outpace terrible climates, fiendish viruses and hungry predators. Behind the scenes, DNA replicates and throws up mutations, and along the way, some of these give rise to remarkable abilities that give the runners a competitive edge. But what if biology doesn’t always work that way? What if nature’s most intricate creations were not painstakingly assembled but more casually dreamed up?

According to Terry Deacon, complexity isn’t always a gift to the fit, but rather more often to the lazy or the lucky. Deacon, a well-regarded professor of biological anthropology and linguistics at the University of California, Berkeley, is interested in natural selection, not so much for what it does, but what happens to species without it. He argues that the absenceof natural selection is an important and unrecognised force in evolution. In fact, he says, when selection pressures lift, genomes go wandering and a suite of unexpected, colourful and synergistic effects can arise. He believes these include not just the Bengalese finch’s song but also some of our own extraordinary physical and mental attributes, including our technological brilliance and our talent for language. If so, then we may have to change our views about our species: far from being a pinnacle of evolution, Deacon sees us more as a “degenerate ape”.

Natural selection, first identified by Charles Darwin in On the Origin of Species,occurs when genetic mutations cause changes in the body and behaviour of an animal that affect its ability to survive and pass on its genes. Some mutations will have positive effects, others may kill an animal outright or somehow affect its offspring’s ability to survive and reproduce. Harsh climates, sparse food and relentless predators destroy many individuals, leaving only those that survive best under exactly those pressures. As a result, the more intense the pressure of natural selection, the tighter the fit between a species and its niche.

So, what happens when the pressure is off? You might think there would be little impetus to adapt, so that species would pretty much stay the same. Not so, says Deacon. Animals still change because genes mutate all the time. The constant rewriting of DNA supplies the raw material from which natural selection picks its winners and losers, and when selection is relaxed, the process of weeding out is less ferocious. Instead, a process calledgenetic drift kicks in as mutations proliferate and animals with a much wider variety of traits are able to survive and reproduce. Some of the classic traits of a species may be lost, while others can arise for no reason other than that it simply doesn’t matter if they do.

Such a process, says Deacon, explains the song of the Bengalese finch. When the bird was raised in a human environment, the pressures that had kept the wild munia’s simple song intact – such as the need to mate, forage and find shelter – were lifted. When the inevitable mutations that affected the bird’s song arose, they persisted because they did not threaten its survival. As a result, the finch’s song now has more notes than the munia’s, is less predictable, and has a kind of syntax. What’s more, while the munia’s song is hard-wired, the finch has to learn its song and uses far more of its brain to create and control it than does the wild bird. By widening the bottleneck on survival, domestication may help explain why the finch’s song changed, but why did it become more complex rather than less?

In the normal course of an animal’s development, Deacon says, the trip from infancy to maturity can be thought of as an accumulation of constraints. Genes are expressed, a body is built, the brain learns and adapts, and the whole thing eventually syncs together to create an adult. As more genes get expressed, and their consequences are superimposed one upon another, an individual becomes “differentiated”, developing into a more specialised creature, he says. But relaxed selection degrades the process of differentiation. “It allows mutations to modify certain genes and inactivate others so they don’t have such a specific function.” Crucially, when an animal’s genes become dedifferentiated, so do traits associated with those genes – from straightforward aspects of the body to more complicated functions involving the brain. “There’s going to be more flexibility,” says Deacon. “Or to put it the other way around, there’s going to be less specificity.”

Going for a Song

As Deacon sees it, when selection on the munia relaxed, it disrupted the tight control certain genes had over brain development, and the neural control over song structure loosened up accordingly. When this happened, other parts of the brain were able to affect the development and practice of the song. This, in turn, made the song vulnerable to influences filtered through the brain, such as the bird’s experience of its environment. The result is a song that is more flexible, more complex and is learned rather than innate.

This “something for nothing” analysis may sound counter-intuitive, but Deacon’s way of thinking is bolstered by a recent computer simulation run by Graham Ritchie and Simon Kirby at the University of Edinburgh, UK. They showed that in a population in which survival depended on software agents recognising each other’s song, the result was simple, unvarying songs. In another trial intended to represent domestication, the experimenters loosened up selection on the song by allowing agents to choose mates randomly regardless of their songs. As a result, the agents developed more complex and varied songs, which led to innovation and change over generations.

“One of the interesting things about relaxed selection that people don’t normally pay attention to is that it’s really easy to accumulate noise that breaks things down,” says Deacon. “Relaxed selection can produce rapid change. In contrast, it’s really hard to accumulate a specific change by natural selection that makes a specific better function.”

Domestication is not the only route to relaxed selection. It can also happen becauseof shifts in climate, changes in an animal’s diet and changes in competitors or predators. Deacon points out that a very generalised kind of relaxed selection may occur when an animal moves into a new environment free of competitors. Then, all individuals can freely reproduce and genetic drift plays a much larger role in shaping the gene pool of the species.

“One of the most striking examples of this phenomenon,” says Deacon, “is the rapid expansion of hominids into most of the Old World, first with Homo erectus at 1.7 million years and then again with Homo sapiensbetween 80,000 and 60,000 years ago.” In terms of human evolution, this may have been a crucial stage in a process of dedifferentiation that primed our genome to allow our startling behavioural complexity.

The most intriguing form of relaxed selection, however, occurs when an animal actively creates a shield against natural selection. This so-called Baldwinian evolution has played a particularly important role in the evolution of our own species. For example, the technological innovations of producing stone tools and cooking meant that our ancestors no longer had to chew tough vegetation and meat. This reshaped the way we look. “There was a radical reduction in large flat molars, thick enamel, robust face and jaw structure and powerful jaw muscles,” says Deacon. Then came agriculture, which made foods evenmore palatable, relaxing the selection pressures on our digestive system. As digestion became easier, more energy was available for other purposes, especially for building and running a larger brain. Our ancestors would have used this increased cognitive capacity, in turn, to devise more technological and cultural innovations to further shield them from the pressures of natural selection.

By this way of thinking, relaxed selection is part of a larger evolutionary dynamic that also incorporates the effects of natural selection. Relaxed selection allows a species to generate diverse traits, and natural selection may laterbe instrumental in further shaping those traits or others that become important in the new evolutionary niche. Deacon believes that each innovation in tool technology, for example, would have brought a major relaxation of pressure on some traits together with unprecedented selection on others.

According to Deacon, human language is the most strikingly complex product of this evolutionary dynamic. Like the Bengalese finch’s song, language is complex, it is learned, there is variation in its use between individuals as well as cultures and it is also massively distributed across thebrain: many separate neural components must work together when we speak.

Deacon believes that language was able to emerge because cultural and technological innovation eased the selection pressures our ancestors faced, in much the same way that domestication relaxed selection in the finches. Deacon suggests that, like the finch’s song, our ancestors’ ancient calls were decoupled from strict genetic control, thus opening the door to the layered influences of other neural systems.

Babbling in human infants is an example of this. Babbling babies produce noise that ranges across the sounds of all human languages, whatever language their parents speak. Unlike other animals that typically vocalise when emotionally aroused, babies babble when they are relaxed. Disinhibited vocalisation, says Deacon, is part of a larger story of language in all its complexity emerging from genes losing their specific functions as a result of relaxed selection.

Others are not so keen to remove the focus from natural selection. “Deacon may be right that relaxed selection played an important role in human evolution, but it’s hard to imagine what evidence we could bring to bear on this,” says anthropologist Richard Klein from Stanford University in California. “I think positive selection for some aspect of cognition or communication underlay the out-of-Africa expansion,” he adds.

Language expert Philip Lieberman from Brown University in Providence, Rhode Island, sees no need for a relaxed selection explanation at all. “The factors that Deacon cites that structure human intelligence would all be selected for through normal Darwinian natural selection,” he says.

Given Deacon’s radical take on human evolution in particular, it is hardly surprising that his ideas are making waves. He does not merely reverse our sense of what complexity is, he upends some of the most basic assumptions we have about ourselves. Instead of being “genetically augmented apes”, he suggests we should think of ourselves as a degenerate species; instead of being forged in the struggle to survive, many of our proudest attributes emerged while we were lazing about in an evolutionary cul-de-sac. ●

Language emerged when technical innovation eased selection pressures on our ancestors, Deacon says.

“Instead of genetically augmented apes we should think of ourselves as a degenerate species”

A fruitful Change

Removing the pressure of natural selection results in the corruption of genes that are no longer required to perform their job faultlessly. Sometimes the degradation may have unexpected knock-on effects: just as some traits are shielded from selection, others may feel its effects more keenly. As a result, marvellous evolutionary innovation may arise. Witness the story of vitamin C.

About 35 million years ago, our primate ancestors stopped eating insects and incorporated a lot more fruit in their diets. Ingesting so much vitamin C meant that individuals no longer needed to make their own. Today, if we don’t get enough vitamin C we die.

We still possess a gene called GULO,which produces the vitamin in other mammals, but our version carriesso many mutations that it is no longer functional. It took a random walk away from its job because it wasn’t kept in place by natural selection, says Terry Deacon from the University of California, Berkeley.

However, as our ancestors lost the ability to produce their own vitamin C, their ability to find and ingest fruit would have become critically important, says Deacon. Those who were most successful at this would have lived longer and produced more offspring, thereby spreading any heritable traits that helped them acquire the vitamin. This, according to Deacon, might partly explain the evolution of three-colour vision, allowing perception of a wide range of the spectrum, as well as changes in teeth and digestion that have since become characteristic of our species.

The relaxed gene

When natural selection takes a back seat, a gene or set of genes may no longer be required to perform a specific job. A common way this happens is when extra copies of a gene are accidentally created during reproduction. Although duplicates are unlikely to make an individual fitter, they may be passed down the generations if their presence does not actively harm their chances of survival. Later, duplicates may acquire mutations of their own and possibly new functions – and if selection becomes more stringent, the new traits may positively aid the creature’s evolutionary success.

Gene duplication constitutes a kind of biological brainstorming – a creative generation of genetic material – and the consequences of this are visible ingenomes. One common outcome is that the job of the original gene is broken up and spread across the new ones. Many gene families, including the HOX family, which builds and segments bodies in development, result from duplication accidents in the distant past. Sometimes the number of copies of the same gene affects a trait. This is true for the human gene for the enzyme amylase, which breaks down starch. Some populations have more copies of the gene than others, and the more you have, the easier it is to process starch (Nature Genetics,vol 39, p 1256). The story of that gene is in its early stages, but as evolution continues, some of the extra copies may be degraded or modified to carry out different functions in concert with the original gene.

Christine Kenneally is the author of The First Word: The search for the origins of language

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