COVER STORY

Adapt first, mutate later Evolution is meant to start with random mutations. But we may have things the wrong way round, reports Colin Barras

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150117_F_Evolving.indd 26 2015-01-12 11:00 “ O BE honest, I was intrigued to see their fins closer to their bodies, lifted their biologists think this kind of plasticity may if they’d even survive on land,” says heads higher off the ground and slipped also play a key role in evolution. Instead of TEmily Standen. Her plan was to drain an less than fish raised in water. Even more mutating first and adapting later, they argue, aquarium of nearly all the water and see how remarkably, their skeletons changed too. animals often adapt first and mutate later. the fish coped. The fish in question were bichir Their “shoulder” bones lengthened and Experiments like Standen’s suggest this fish that can breathe air and haul themselves developed stronger contacts with the fin process could even play a role in major over land when they have to, so it’s not as far- bones, making the fish better at press-ups. evolutionary transitions such as fish taking fetched as it sounds. The bone attachments to the skull also to land and apes starting to walk upright. What was perhaps more questionable weakened, allowing the head to move more. The idea that plasticity plays a role in was Standen’s rationale. Two years earlier, These features are uncannily reminiscent evolution goes back more than a century. in 2006, Tiktaalik had become a global of those that occurred as our four-legged Some early biologists thought that sensation. This 360-million-year-old fossil ancestors evolved from Tiktaalik-like forebears. characteristics acquired during an animal’s provides a snapshot of the moment our fishy What is really amazing about this lifetime could be inherited by their offspring: ancestors hauled themselves out of the water experiment is that these changes did not come giraffes got their long necks by stretching to and began trading fins for limbs. Standen about after raising generations of fish on land eat leaves, and so on. The French naturalist thought forcing bichir fish to live almost and allowing only the best walkers to breed. Jean-Baptiste Lamarck is the best-known entirely on land could reveal more about Instead, it happened within the lifetime of advocate of this idea, but Darwin believed this crucial step in our evolution. Even individual fish. Simply forcing young fish to something similar. He even proposed if you were being kind, you might have live on land for eight months was all it took an elaborate mechanism to explain how described this notion as a little bit fanciful. to produce these quite dramatic changes. information about changes in the body Today, it seems positively inspired. The We have long known that our muscles, could reach eggs and sperm, and therefore bichirs did far more than just survive. They sinews and bones adapt to cope with whatever be passed on to offspring. In this way, Darwin

MORGAN SCHWEITZER MORGAN became better at “walking”. They planted we make them do. A growing number of suggested, plasticity produces the heritable >

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150117_F_Evolving.indd 27 2015-01-12 11:00 variations on which natural selection can Evolving without evolving work its magic. With the rise of modern genetics, such notions were dismissed. It became clear Standard model: mutate frst, adapt later that there is no way for information about Mutation in egg or sperm Mutation produces physical Mutation spreads if advantageous what animals do during their lifetime to changes in ofspring be passed on to their offspring (although a few exceptions have emerged since). And it was thought this meant plasticity has no role in evolution. Instead, the focus shifted to mutations. By the 1940s, the standard thinking was that animals mutate first and adapt later. A mutation in a sperm cell, say, might produce a physical change in the bodies of Genetic assimilation: adapt frst, mutate later some offspring. If the change is beneficial, No mutation at frst Physical changes are a plastic Only later do mutations “fx” the mutation will spread through the response to a diferent the physical changes population. In other words, random genetic environment mutations generate the variation on which natural selection acts. This remains the dominant view of evolution today. The dramatic effects of plasticity were not entirely ignored. In the 1940s, for instance, the Dutch zoologist Everhard Johannes Slijper studied a goat that had been born without forelegs and learned to hop around, kangaroo-like, on its rear legs. of heritable changes. “You can plastically When Slijper examined the goat after its induce generation after generation,” says death, he discovered that the shape of its Standen, who is now at the University of muscles and skeleton looked more like Ottawa in Ontario, Canada. “At some point, those of a biped than a quadruped. can you remove the environmental Few biologists considered such findings conditions that induced the change and relevant to the evolutionary process. The have the organisms remain changed?” fact that changes acquired during an animal’s The answer, surprisingly, seems to be yes. lifetime are transient seemed to rule out that In the 1950s, British biologist Conrad Hal No coincidence possibility. If Standen’s better-at-walking fish Waddington showed that it is feasible in an Can plasticity explain why were bred and the offspring raised in a normal experiment involving fruit flies. Waddington evolution repeats itself? aquarium, for instance, they should look and found that when pupa are briefly heated, behave like perfectly ordinary bichirs. some offspring develop without crossveins During the last ice age, great ice in their wings. He then selected and bred those sheets covered much of Eurasia and flies. By the 14th generation, some lacked North America. As they retreated, Transient response crossveins even when their pupa were not they left behind lakes and rivers But what if the environmental conditions that heated. A physical feature that began as a with no native fish. induce the plastic response are themselves plastic response to an environmental trigger Marine three-spined sticklebacks permanent? In the wild, this could happen as had become a hereditary feature. were quick to take advantage, a result of alterations in prey animals, or in the How is this possible? Plastic changes occur repeatedly colonising these new climate, for instance. Then all the members because an environmental trigger affects a environments and evolving into the of a population would develop in the same, developmental pathway in some way. More freshwater sticklebacks found today consistent way down the generations. It of a certain hormone may be produced, or (pictured right). What’s extraordinary, would look as if the population had evolved produced at a different time, or genes are though, is that freshwater species in response to an altered environment, but switched on that normally remain inactive, that evolved entirely independently technically it’s not evolution because there and so on. The thing is, random mutations can of each other are often strikingly is no heritable change. The thing is, the only also have similar effects. So in an environment similar in body shape, and so on. way to tell would be to “test” individuals by in which a particular plastic response is crucial This is far from the only example. raising them in different circumstances. for survival, only mutations that reinforce The cichlid fish of Africa’s lakes, for In this way at least, plasticity can allow this response, or at least do not impede it, instance, have also evolved along animals to “evolve” without evolving. The can spread through a population. Eventually, parallel lines in many cases. crucial question, of course, is whether it the altered developmental pathway will The standard explanation for this can lead to actual evolution, in the sense become so firmly stabilised by a genetic is convergent evolution: even though

28 | NewScientist | 17 January 2015 scaffolding that it will occur even without rethink (Nature, vol 514, p 161). Most biologists University in Durham, North Carolina. the environmental trigger, making it a have yet to be convinced. “But there is unfortunately very little support permanent hereditary feature. The sceptics point out that genetic for its role in nature.” This is what makes Waddington called this process genetic assimilation does not overturn any Standen’s work on the bichir so significant. assimilation. It may sound like Lamarckism, fundamental principles of evolution – in It implicates plasticity in a major evolutionary but it is not. The acquired characteristics the long run, evolution is all about the spread transition: fish turning into four-legged land don’t shape the genetic changes directly as of mutations, whether or not plasticity is animals (Nature, vol 513, p 54). Darwin proposed, they merely allow animals involved. Yes, say the proponents of plasticity, Plasticity will soon be implicated in another to thrive in environments that favour certain major transition too – the one our ancestors mutations when they occur by chance. “ The ‘bipedal’ mice had made from four legs to two about 7 million Waddington’s findings have been regarded years ago. Adam Foster, now at the Northeast as a curiosity rather than a crucial insight. But features like those in our Ohio Medical University in Rootstown, has in the past decade or two, attitudes have begun hominin ancestors” been making mice walk on a treadmill. “I had a to change. One reason for this is a growing custom harness system built so I could modify appreciation of the flexibility of genes. Rather but the key point is that plasticity can the load experienced by the hind limbs,” he than being rigidly preprogrammed, we now determine which mutations spread (New says. Some mice had to walk on their hind know that the environment influences many Scientist, 12 October 2013, p 33), so its role limbs, while others walked on all fours. Each aspects of animals’ bodies and behaviour. should be given the prominence it deserves. mouse exercised on the treadmill for an hour Such discoveries have led some biologists “Several major recent evolutionary textbooks a day for three months, and then Foster to claim that developmental plasticity plays do not even mention plasticity,” says Laland. examined their skeletons. a major role in evolution. A few, such as Kevin It may play a role occasionally, respond He found that the “bipedal” mice had Laland at the University of St Andrews, UK, the sceptics, but it’s a minor one at best. developed longer legs than standard even argue that the conventional “mutate “There is little debate that genetic assimilation quadrupedal mice, and that their thigh first, adapt later” picture of evolution needs a can happen,” says Gregory Wray of Duke bones had larger femoral heads – the ball in >

mutations are random, similar that occurred as their ancestors environments produce similar moved into new environments. And evolutionary results. And there is this is actually a testable prediction some evidence to support this view, when it comes to freshwater for instance when it comes to the sticklebacks; marine three-spined loss of armour plates in freshwater sticklebacks are still around, and stickleback species (New Scientist, have changed little since the ice age. 2 April 2011, p 32). So Matthew Wund at The College of New Jersey in Ewing decided to put Strikingly similar West-Eberhard’s ideas to the test. But Mary Jane West-Eberhard of With colleagues at Clark University in the Smithsonian Tropical Research Worcester, Massachusetts, he set out Institute in Costa Rica thinks to discover whether simply allowing parallel evolution happens too marine sticklebacks to eat a diet often for convergence to be the similar to those of their freshwater full explanation. In her 2003 book cousins as they grew up would lead Environmental Plasticity and them to develop similar body shapes Evolution, she argues that it happens too. And it did.

because similar conditions produce Marine fish raised on planktonic BOOTH/SCIENCE SIMON LIBRARY PHOTO a similar plastic response in the invertebrates from the upper water ancestral species. Natural selection of deep lakes developed the long of sticklebacks that live there (The experiments, published a couple of then reinforces those trajectories. snouts of sticklebacks living in American Naturalist, vol 172, p 449). years ago, also support the idea that If West-Eberhard is right, then lake surface waters. In contrast, “We subsequently expanded the developmental plasticity shaped at least some of the heritable marine fish given large invertebrates experiment to consider not only the evolution of sticklebacks as characteristics seen in living animals found at the bottom of shallow lakes dietary differences but also habitat,” they invaded the lakes left by the originated from the plastic changes developed the stubby snouts typical says Wund. The results of those retreating ice sheets.

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150117_F_Evolving.indd 29 2015-01-12 11:00 the hip joint. Both features are associated with the transition to bipedalism in our hominin ancestors. Foster’s results will be published later this year. “I think Adam’s research is really compelling,” says Jesse Young, an anatomist at Northeast Ohio Medical University. “As he was getting it going, I was a bit sceptical. You couldn’t predict it would reveal anything useful.” While the work of Standen and Foster suggests that developmental plasticity could play a role in major evolutionary transitions, it is only suggestive. Indeed, these studies do not even show that the plastic changes seen in the bichir fish and mice can be fixed by mutations. Demonstrating this kind of genetic assimilation would certainly be tricky, says Standen. It would not be practical with the bichir fish she studied. “As wonderful as they are, they’re frustrating

fish,” says Standen. “They take the better part Y of a decade to mature, and even then they’re TT RD/GE

really difficult to breed in captivity.” A Fiddler crabs can The fossil record is usually no help either. take either side in ERNH B S

It is possible that some of the changes seen A the debate about

as fish colonised the land were a result of TOBI the role of plasticity plasticity rather than genetics, says Per Ahlberg of the University of Uppsala in UK. “We just don’t because we’re not as active.” hereditary asymmetries that appeared on Sweden who studies the transition to land. It’s possible that similar kinds of skeletal either side (Science, vol 306, p 828). “I think For Ahlberg, the trouble is that there is no structural change seen in prehistory have it’s one of the clearest demonstrations that way to prove it. “There’s no evidence that will been misinterpreted as signs of speciation genetic assimilation has happened and that it allow us to choose between the two,” he says. when they really just reflect developmental is more common than expected,” says Palmer. plasticity, says Shaw – perhaps especially so There is a caveat here, though. The ancestral in hominin evolution. Humans are unique, non-hereditary asymmetries may have been a More evolvable he points out. “Our first line of defence against result of random genetic noise, says Palmer. So Other biologists are more enthusiastic. It has environmental insult is culture. When that’s while his work does show genetic assimilation long been suggested that different parts of the not adequate – for instance if the clothing you in action, it was not necessarily fixing traits skeleton are more plastic and “evolvable” than can make is not good enough to keep you due to developmental plasticity. others, says William Harcourt-Smith of the warm – then arguably the second line of There is no simple way to prove the American Museum of Natural History. “So a defence is plasticity. Only after that fails evolutionary importance of developmental foot bone or a hand bone might give you more might you actually get genetic selection.” plasticity, says Mary Jane West-Eberhard of the useful info than a hip bone, for instance.” All this still leaves open the question of Smithsonian Tropical Research Institute in Work like Foster’s could reveal if this is whether genetic assimilation can “fix” traits Costa Rica, whose work has been particularly indeed the case and help us interpret the that first appear as a result of plasticity. A influential. “Evolutionary biology that is fossil record of human evolution. “These decade ago, Richard Palmer at the University concerned with evolution and speciation in experiments do have validity,” Harcourt- of Alberta in Edmonton, Canada, found a way nature necessarily depends on indirect proof – Smith says. “They can help us understand to search for evidence in the fossil record. an accumulation of facts that support or deny whether traits are plastic or not.” Most animals have some asymmetric a hypothesis,” she says. Take the honeycomb structure in the heads traits. In our case, it’s the position of the At the moment, the facts that are of our long bones. It is lighter and weaker heart and other organs, which is encoded in accumulating seem to support the hypothesis. than it was in our extinct cousins such as our genes. But in other species, asymmetries Expect lots more results soon: Standen’s the Neanderthals. A study out last month are plastic. For instance, the enlarged claw success is inspiring others. “I’ve already had compared the bones of hunter-gatherers and of male fiddler crabs (pictured above) is as people ask me what other critters we could try early farmers in North America. It concluded likely to be on the left as on the right. this on,” says Standen. “Everybody is friendly that our bones became weak only when our What Palmer showed by examining and excited and interested. It’s fun – it’s the ancestors’ lifestyles changed (PNAS, doi.org/ the fossil record of asymmetry in 68 plant way science should be.” ■ xwq). “We could have a skeleton as strong as and animal species is that on 28 occasions, our prehistoric ancestors,” says team member asymmetries that are now hereditary and Colin Barras is a freelance writer based in Ann Colin Shaw of the University of Cambridge, appear only on one side started out as non- Arbor, Michigan

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