Strange as it sounds, scientists still do not know the answers to some of the most basic questions about how life on Earth evolved. Take eyes, for instance. Where do they come from, exactly? The usual explanation of how we got these stupendously complex organs rests upon the theory of natural selection.

You may recall the gist from school biology lessons. If a creature with poor eyesight happens to produce offspring with slightly better eyesight, thanks to random mutations, then that tiny bit more vision gives them more chance of survival. The longer they survive, the more chance they have to reproduce and pass on the genes that equipped them with slightly better eyesight. Some of their offspring might, in turn, have better eyesight than their parents, making it likelier that they, too, will reproduce. And so on. Generation by generation, over unfathomably long periods of time, tiny advantages add up. Eventually, after a few hundred million years, you have creatures who can see as well as humans, or cats, or owls.

This is the basic story of evolution, as recounted in countless textbooks and pop-science bestsellers. The problem, according to a growing number of scientists, is that it is absurdly crude and misleading.

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For one thing, it starts midway through the story, taking for granted the existence of light-sensitive cells, lenses and irises, without explaining where they came from in the first place. Nor does it adequately explain how such delicate and easily disrupted components meshed together to form a single organ. And it isnt just eyes that the traditional theory struggles with. The first eye, the first wing, the first placenta. How they emerge. Explaining these is the foundational motivation of evolutionary biology, says Armin Moczek, a biologist at Indiana University. And yet, we still do not have a good answer. This classic idea of gradual change, one happy accident at a time, has so far fallen flat.

There are certain core evolutionary principles that no scientist seriously questions. Everyone agrees that natural selection plays a role, as does mutation and random chance. But how exactly these processes interact and whether other forces might also be at work has become the subject of bitter dispute. If we cannot explain things with the tools we have right now, the Yale University biologist Gnter Wagner told me, we must find new ways of explaining.

In 2014, eight scientists took up this challenge, publishing an article in the leading journal Nature that asked Does evolutionary theory need a rethink? Their answer was: Yes, urgently. Each of the authors came from cutting-edge scientific subfields, from the study of the way organisms alter their environment in order to reduce the normal pressure of natural selection think of beavers building dams to new research showing that chemical modifications added to DNA during our lifetimes can be passed on to our offspring. The authors called for a new understanding of evolution that could make room for such discoveries. The name they gave this new framework was rather bland the Extended Evolutionary Synthesis (EES) but their proposals were, to many fellow scientists, incendiary.

In 2015, the Royal Society in London agreed to host New Trends in Evolution, a conference at which some of the articles authors would speak alongside a distinguished lineup of scientists. The aim was to discuss new interpretations, new questions, a whole new causal structure for biology, one of the organisers told me. But when the conference was announced, 23 fellows of the Royal Society, Britains oldest and most prestigious scientific organisation, wrote a letter of protest to its then president, the Nobel laureate Sir Paul Nurse. The fact that the society would hold a meeting that gave the public the idea that this stuff is mainstream is disgraceful, one of the signatories told me. Nurse was surprised by the reaction. They thought I was giving it too much credibility, he told me. But, he said: Theres no harm in discussing things.

Traditional evolutionary theorists were invited, but few showed up. Nick Barton, recipient of the 2008 Darwin-Wallace medal, evolutionary biologys highest honour, told me he decided not to go because it would add more fuel to the strange enterprise. The influential biologists Brian and Deborah Charlesworth of the University of Edinburgh told me they didnt attend because they found the premise irritating. The evolutionary theorist Jerry Coyne later wrote that the scientists behind the EES were playing revolutionaries to advance their own careers. One 2017 paper even suggested some of the theorists behind the EES were part of an increasing post-truth tendency within science. The personal attacks and insinuations against the scientists involved were shocking and ugly, said one scientist, who is nonetheless sceptical of the EES.

What accounts for the ferocity of this backlash? For one thing, this is a battle of ideas over the fate of one of the grand theories that shaped the modern age. But it is also a struggle for professional recognition and status, about who gets to decide what is core and what is peripheral to the discipline. The issue at stake, says Arlin Stoltzfus, an evolutionary theorist at the IBBR research institute in Maryland, is who is going to write the grand narrative of biology. And underneath all this lurks another, deeper question: whether the idea of a grand story of biology is a fairytale we need to finally give up.

Behind the current battle over evolution lies a broken dream. In the early 20th century, many biologists longed for a unifying theory that would enable their field to join physics and chemistry in the club of austere, mechanistic sciences that stripped the universe down to a set of elemental rules. Without such a theory, they feared that biology would remain a bundle of fractious sub-fields, from zoology to biochemistry, in which answering any question might require input and argument from scores of warring specialists.

From todays vantage point, it seems obvious that Darwins theory of evolution a simple, elegant theory that explains how one force, natural selection, came to shape the entire development of life on Earth would play the role of the great unifier. But at the turn of the 20th century, four decades after the publication of On the Origin of Species and two after his death, Darwins ideas were in decline. Scientific collections at the time carried titles such as The Death-bed of Darwinism. Scientists had not lost interest in evolution, but many found Darwins account of it unsatisfying. One major problem was that it lacked an explanation of heredity. Darwin had observed that, over time, living things seemed to change to better fit their environment. But he did not understand how these minute changes were passed from one generation to the next.

At the start of the 20th century, the rediscovery of the work of the 19th-century friar and father of genetics, Gregor Mendel, started to provide the answers. Scientists working in the new field of genetics discovered rules that governed the quirks of heredity. But rather than confirm Darwins theory, they complicated it. Reproduction appeared to remix genes the mysterious units that programme the physical traits we end up seeing in surprising ways. Think of the way a grandfathers red hair, absent in his son, might reappear in his granddaughter. How was natural selection meant to function when its tiny variations might not even reliably pass from parent to offspring every time?

Even more ominous for Darwinists was the emergence of the mutationists in the 1910s, a school of geneticists whose star exponent, Thomas Hunt Morgan, showed that by breeding millions of fruit flies and sometimes spiking their food with the radioactive element radium he could produce mutated traits, such as new eye colours or additional limbs. These were not the tiny random variations on which Darwins theory was built, but sudden, dramatic changes. And these mutations, it turned out, were heritable. The mutationists believed that they had identified lifes true creative force. Sure, natural selection helped to remove unsuitable changes, but it was simply a humdrum editor for the flamboyant poetry of mutation. Natura non facit saltum, Darwin had once written: Nature does not make jumps. The mutationists begged to differ.

These disputes over evolution had the weight of a theological schism. At stake were the forces governing all creation. For Darwinists especially, their theory was all-or-nothing. If another force, apart from natural selection, could also explain the differences we see between living things, Darwin wrote in On the Origin of Species, his whole theory of life would utterly break down. If the mutationists were right, instead of a single force governing all biological change, scientists would have to dig deep into the logic of mutation. Did it work differently on legs and lungs? Did mutations in frogs work differently to mutations in owls or elephants?

In 1920, the philosopher Joseph Henry Woodger wrote that biology suffered from fragmentation and cleavages that would be unknown in such a well-unified science as, for example, chemistry. The divergent groups often feuded, he noted, and it seemed to be getting worse. It began to seem inevitable that the life sciences would grow more and more fractured, and the possibility of a common language would slip away.

Just as it seemed that Darwinism might be buried, a curious collection of statisticians and animal breeders came along to revitalise it. In the 1920s and 30s, working separately but in loose correspondence, thinkers such as the British father of scientific statistics, Ronald Fisher, and the American livestock breeder Sewall Wright, proposed a revised theory of evolution that accounted for scientific advances since Darwins death but still promised to explain all of lifes mysteries with a few simple rules. In 1942, the English biologist Julian Huxley coined the name for this theory: the modern synthesis. Eighty years on, it still provides the basic framework for evolutionary biology as it is taught to millions of schoolchildren and undergraduates every year. Insofar as a biologist works in the tradition of the modern synthesis, they are considered mainstream; insofar as they reject it, they are considered marginal.

Despite the name, it was not actually a synthesis of two fields, but a vindication of one in light of the other. By building statistical models of animal populations that accounted for the laws of genetics and mutation, the modern synthesists showed that, over long periods of time, natural selection still functioned much as Darwin had predicted. It was still the boss. In the fullness of time, mutations were too rare to matter, and the rules of heredity didnt affect the overall power of natural selection. Through a gradual process, genes with advantages were preserved over time, while others that didnt confer advantages disappeared.

Rather than getting stuck into the messy world of individual organisms and their specific environments, proponents of the modern synthesis observed from the lofty perspective of population genetics. To them, the story of life was ultimately just the story of clusters of genes surviving or dying out over the grand sweep of evolutionary time.

The modern synthesis arrived at just the right time. Beyond its explanatory power, there were two further reasons more historical, or even sociological, than scientific why it took off. First, the mathematical rigour of the synthesis was impressive, and not seen before in biology. As the historian Betty Smocovitis points out, it brought the field closer to examplar sciences such as physics. At the same time, writes Smocovitis, it promised to unify the life sciences at a moment when the enlightenment project of scientific unification was all the rage. In 1946, the biologists Ernst Mayr and George Gaylord Simpson started the Society for the Study of Evolution, a professional organisation with its own journal, which Simpson said would bring together the sub-fields of biology on the common ground of evolutionary studies. This was all possible, he later reflected, because we seem at last to have a unified theory [] capable of facing all the classic problems of the history of life and of providing a causalistic solution of each.

This was a time when biology was ascending to its status as a major science. University departments were forming, funding was flowing in, and thousands of newly accredited scientists were making thrilling discoveries. In 1944, the Canadian-American biologist Oswald Avery and his colleagues had proved that DNA was the physical substance of genes and heredity, and in 1953 James Watson and Francis Crick leaning heavily on work from Rosalind Franklin and the American chemist Linus Pauling mapped its double-helical structure.

While information piled up at a rate that no scientist could fully digest, the steady thrum of the modern synthesis ran through it all. The theory dictated that, ultimately, genes built everything, and natural selection scrutinised every bit of life for advantage. Whether you were looking at algae blooming in a pond or peacock mating rituals, it could all be understood as natural selection doing its work on genes. The world of life could seem suddenly simple again.

By 1959, when the University of Chicago held a conference celebrating the centennial of the publication of On the Origin of Species, the modern synthesists were triumphant. The venues were packed and national newspaper reporters followed the proceedings. (Queen Elizabeth was invited, but sent her apologies.) Huxley crowed that this is one of the first public occasions on which it has been frankly faced that all aspects of reality are subject to evolution.

Yet soon enough, the modern synthesis would come under assault from scientists within the very departments that the theory had helped build.

From the start, there had always been dissenters. In 1959, the developmental biologist CH Waddington lamented that the modern synthesis had sidelined valuable theories in favour of drastic simplifications which are liable to lead us to a false picture of how the evolutionary process works. Privately, he complained that anyone working outside the new evolutionary party line that is, anyone who didnt embrace the modern synthesis was ostracised.

Then came a devastating series of new findings that called into question the theorys foundations. These discoveries, which began in the late 60s, came from molecular biologists. While the modern synthesists looked at life as if through a telescope, studying the development of huge populations over immense chunks of time, the molecular biologists looked through a microscope, focusing on individual molecules. And when they looked, they found that natural selection was not the all-powerful force that many had assumed it to be.

They found that the molecules in our cells and thus the sequences of the genes behind them were mutating at a very high rate. This was unexpected, but not necessarily a threat to mainstream evolutionary theory. According to the modern synthesis, even if mutations turned out to be common, natural selection would, over time, still be the primary cause of change, preserving the useful mutations and junking the useless ones. But that isnt what was happening. The genes were changing that is, evolving but natural selection wasnt playing a part. Some genetic changes were being preserved for no reason apart from pure chance. Natural selection seemed to be asleep at the wheel.

Evolutionary biologists were stunned. In 1973, David Attenborough presented a BBC documentary that included an interview with one of the leading modern synthesists, Theodosius Dobzhansky. He was visibly distraught at the non-Darwinian evolution that some scientists were now proposing. If this were so, evolution would have hardly any meaning, and would not be going anywhere in particular, he said. This is not simply a quibble among specialists. To a man looking for the meaning of his existence, evolution by natural selection makes sense. Where once Christians had complained that Darwins theory made life meaningless, now Darwinists levelled the same complaint at scientists who contradicted Darwin.

Other assaults on evolutionary orthodoxy followed. The influential palaeontologists Stephen Jay Gould and Niles Eldredge argued that the fossil record showed evolution often happened in short, concentrated bursts; it didnt have to be slow and gradual. Other biologists simply found that the modern synthesis had little relevance to their work. As the study of life increased in complexity, a theory based on which genes were selected in various environments started to seem beside the point. It didnt help answer questions such as how life emerged from the seas, or how complex organs, such as the placenta, developed. Using the lens of the modern synthesis to explain the latter, says the Yale developmental biologist Gnter Wagner, would be like using thermodynamics to explain how the brain works. (The laws of thermodynamics, which explain how energy is transferred, do apply to the brain, but they arent much help if you want to know how memories are formed or why we experience emotion.)

Just as feared, the field split. In the 70s, molecular biologists in many universities peeled off from biology departments to form their own separate departments and journals. Some in other sub-fields, such as palaeontology and developmental biology, drifted away as well. Yet the biggest field of all, mainstream evolutionary biology, continued much as before. The way the champions of the modern synthesis who by this point dominated university biology departments dealt with potentially destabilising new findings was by acknowledging that such processes happen sometimes (subtext: rarely), are useful to some specialists (subtext: obscure ones), but do not fundamentally alter the basic understanding of biology that descends from the modern synthesis (subtext: dont worry about it, we can continue as before). In short, new discoveries were often dismissed as little more than mildly diverting curiosities.

Today, the modern synthesis remains, mutatis mutandis, the core of modern evolutionary biology wrote the evolutionary theorist Douglas Futuyma in a 2017 paper defending the mainstream view. The current version of the theory allows some room for mutation and random chance, but still views evolution as the story of genes surviving in vast populations. Perhaps the biggest change from the theorys mid-century glory days is that its most ambitious claims that simply by understanding genes and natural selection, we can understand all life on earth have been dropped, or now come weighted with caveats and exceptions. This shift has occurred with little fanfare. The theorys ideas are still deeply embedded in the field, yet no formal reckoning with its failures or schisms has occurred. To its critics, the modern synthesis occupies a position akin to a president reneging on a campaign promise it failed to satisfy its entire coalition, but remains in office, hands on the levers of power, despite its diminished offer.

Brian and Deborah Charlesworth are considered by many to be high priests of the tradition that descends from the modern synthesis. They are eminent thinkers, who have written extensively on the place of new theories in evolutionary biology, and they dont believe any radical revision is needed. Some argue that they are too conservative, but they insist they are simply careful cautious about dismantling a tried-and-tested framework in favour of theories that lack evidence. They are interested in fundamental truths about evolution, not explaining every diverse result of the process.

Were not here to explain the elephants trunk, or the camels hump. If such explanations could even be possible, Brian Charlesworth told me. Instead, he said, evolutionary theory should be universal, focusing on the small number of factors that apply to how every living thing develops. Its easy to get hung up on you havent explained why a particular system works the way it does. But we dont need to know, Deborah told me. Its not that the exceptions are uninteresting; its just that they arent all that important.

Kevin Laland, the scientist who organised the contentious Royal Society conference, believes it is time for proponents of neglected evolutionary sub-fields to band together. Laland and his fellow proponents of the Extended Evolutionary Synthesis, the EES, call for a new way of thinking about evolution one that starts not by seeking the simplest explanation, or the universal one, but what combination of approaches offers the best explanation to biologys major questions. Ultimately, they want their sub-fields plasticity, evolutionary development, epigenetics, cultural evolution not just recognised, but formalised in the canon of biology.

There are some firebrands among this group. The geneticist Eva Jablonka has proclaimed herself a neo-Lamarckist, after Jean-Baptiste Lamarck, the 19th-century populariser of pre-Darwinian ideas of inheritance, who has often been seen as a punchline in the history of science. Meanwhile, the physiologist Denis Noble has called for a revolution against traditional evolutionary theory. But Laland, a lead author on many of the movements papers, insists that they simply want to expand the current definition of evolution. They are reformers, not revolutionaries.

The case for EES rests on a simple claim: in the past few decades, we have learned many remarkable things about the natural world and these things should be given space in biologys core theory. One of the most fascinating recent areas of research is known as plasticity, which has shown that some organisms have the potential to adapt more rapidly and more radically than was once thought. Descriptions of plasticity are startling, bringing to mind the kinds of wild transformations you might expect to find in comic books and science fiction movies.

Emily Standen is a scientist at the University of Ottawa, who studies Polypterus senegalus, AKA the Senegal bichir, a fish that not only has gills but also primitive lungs. Regular polypterus can breathe air at the surface, but they are much more content living underwater, she says. But when Standen took Polypterus that had spent their first few weeks of life in water, and subsequently raised them on land, their bodies began to change immediately. The bones in their fins elongated and became sharper, able to pull them along dry land with the help of wider joint sockets and larger muscles. Their necks softened. Their primordial lungs expanded and their other organs shifted to accommodate them. Their entire appearance transformed. They resembled the transition species you see in the fossil record, partway between sea and land, Standen told me. According to the traditional theory of evolution, this kind of change takes millions of years. But, says Armin Moczek, an extended synthesis proponent, the Senegal bichir is adapting to land in a single generation. He sounded almost proud of the fish.

Moczeks own area of expertise is dung beetles, another remarkably plastic species. In a cold environment, dung beetles will grow larger wings to range further for food; in a warm one, a rounder body and stomach to gorge locally. The crucial thing about these observations, which challenge the traditional understanding of evolution, is that these sudden developments all come from the same underlying genes. The speciess genes arent being slowly honed, generation by generation. Rather, during its early development it has the potential to grow in a variety of ways, allowing it to survive in different situations.

We believe this is ubiquitous across species, says David Pfennig of the University of North Carolina at Chapel Hill. He works on spadefoot toads, amphibians the size of a Matchbox car. Spadefoots are normally omnivorous, but spadefoot tadpoles raised solely on meat grow larger teeth, more powerful jaws, and a hardy, more complex gut. Suddenly, they resemble a powerful carnivore, feeding on hardy crustaceans, and even other tadpoles.

Plasticity doesnt invalidate the idea of gradual change through selection of small changes, but it offers another evolutionary system with its own logic working in concert. To some researchers, it may even hold the answers to the vexed question of biological novelties: the first eye, the first wing. Plasticity is perhaps what sparks the rudimentary form of a novel trait, says Pfennig.

Plasticity is well accepted in developmental biology, and the pioneering theorist Mary Jane West-Eberhard began making the case that it was a core evolutionary force in the early 00s. And yet, to biologists in many other fields, it is virtually unknown. Undergraduates beginning their education are unlikely to hear anything about it, and it has still to make much mark in popular science writing.

Biology is full of theories like this. Other interests of the EES include extra-genetic inheritance, known as epigenetics. This is the idea that something say a psychological injury, or a disease experienced by a parent attaches small chemical molecules to their DNA that are repeated in their children. This has been shown to happen in some animals across multiple generations, and caused controversy when it was suggested as an explanation for intergenerational trauma in humans. Other EES proponents track the inheritance of things like culture as when groups of dolphins develop and then teach each other new hunting techniques or the communities of helpful microbes in animal guts or plant roots, which are tended to and passed on through generations like a tool. In both cases, researchers contend that these factors might impact evolution enough to warrant a more central role. Some of these ideas have become briefly fashionable, but remain disputed. Others have sat around for decades, offering their insights to a small audience of specialists and no one else. Just like at the turn of the 20th century, the field is split into hundreds of sub-fields, each barely aware of the rest.

To the EES group, this is a problem that urgently needs to be solved and the only solution is a more capacious unifying theory. These scientists are keen to expand their research and gather the data to disprove their doubters. But they are also aware that logging results in the literature may not be enough. Parts of the modern synthesis are deeply ingrained in the whole scientific community, in funding networks, positions, professorships, says Gerd B Mller, head of the Department of Theoretical Biology at the university of Vienna and a major backer of the EES. Its a whole industry.

The modern synthesis was such a seismic event that even its flatly wrong ideas took up to half a century to correct. The mutationists were so thoroughly buried that even after decades of proof that mutation was, in fact, a key part of evolution, their ideas were still regarded with suspicion. As recently as 1990, one of the most influential university evolution textbooks could claim that the role of new mutations is not of immediate significance something that very few scientists then, or now, actually believe. Wars of ideas are not won with ideas alone.

To release biology from the legacy of the modern synthesis, explains Massimo Pigliucci, a former professor of evolution at Stony Brook University in New York, you need a range of tactics to spark a reckoning: Persuasion, students taking up these ideas, funding, professorial positions. You need hearts as well as minds. During a Q&A with Pigliucci at a conference in 2017, one audience member commented that the disagreement between EES proponents and more conservative biologists sometimes looked more like a culture war than a scientific disagreement. According to one attender, Pigliucci basically said: Sure, its a culture war, and were going to win it, and half the room burst out cheering.

To some scientists, though, the battle between traditionalists and extended synthesists is futile. Not only is it impossible to make sense of modern biology, they say, it is unnecessary. Over the past decade the influential biochemist Ford Doolittle has published essays rubbishing the idea that the life sciences need codification. We dont need no friggin new synthesis. We didnt even really need the old synthesis, he told me.

What Doolittle and like-minded scientists want is more radical: the death of grand theories entirely. They see such unifying projects as a mid-century even modernist conceit, that have no place in the postmodern era of science. The idea that there could be a coherent theory of evolution is an artefact of how biology developed in the 20th century, probably useful at the time, says Doolittle. But not now. Doing right by Darwin isnt about venerating all his ideas, he says, but building on his insight that we can explain how present life forms came from past ones in radical new ways.

Doolittle and his allies, such as the computational biologist Arlin Stoltzfus, are descendants of the scientists who challenged the modern synthesis from the late 60s onwards by emphasising the importance of randomness and mutation. The current superstar of this view, known as neutral evolution, is Michael Lynch, a geneticist at the University of Arizona. Lynch is soft-spoken in conversation, but unusually pugnacious in what scientists call the literature. His books rail against scientists who accept the status quo and fail to appreciate the rigorous mathematics that undergirds his work. For the vast majority of biologists, evolution is nothing more than natural selection, he wrote in 2007. This blind acceptance [] has led to a lot of sloppy thinking, and is probably the primary reason why evolution is viewed as a soft science by much of society. (Lynch is also not a fan of the EES. If it were up to him, biology would be even more reductive than the modern synthesists imagined.)

What Lynch has shown, over the past two decades, is that many of the complex ways DNA is organised in our cells probably happened at random. Natural selection has shaped the living world, he argues, but so too has a sort of formless cosmic drifting that can, from time to time, assemble order from chaos. When I spoke to Lynch, he said he would continue to extend his work to as many fields of biology as possible looking at cells, organs, even whole organisms to prove that these random processes were universal.

As with so many of the arguments that divide evolutionary biologists today, this comes down to a matter of emphasis. More conservative biologists do not deny that random processes occur, but believe theyre much less important than Doolittle or Lynch think.

The computational biologist Eugene Koonin thinks people should get used to theories not fitting together. Unification is a mirage. In my view there is no can be no single theory of evolution, he told me. There cannot be a single theory of everything. Even physicists do not have a theory of everything.

This is true. Physicists agree that the theory of quantum mechanics applies to very tiny particles, and Einsteins theory of general relativity applies to larger ones. Yet the two theories appear incompatible. Late in life, Einstein hoped to find a way to unify them. He died unsuccessful. In the next few decades, other physicists took up the same task, but progress stalled, and many came to believe it might be impossible. If you ask a physicist today about whether we need a unifying theory, they would probably look at you with puzzlement. Whats the point, they might ask. The field works, the work continues.

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Do we need a new theory of evolution? - The Guardian