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G ince the turn of the twentieth cen- separate mouth and anus, a central nervous R An obscure group of tiny E B tury, zoologists have set out from system and organs to filter waste. Although L L A W coastal marine stations at dawn to creatures takes centre stage the position of acoels has moved around . sieve peppercorn-sized worms from in a battle to work out the a bit over the decades, a DNA analysis in A Ssea-bottom muck. These creatures, called 1999 (ref. 2) and several since then have acoels, often look like unremarkable splashes tree of life. placed them back in their earlier spot. In of paint when seen through a microscope. But particular, a genetic study of 94 organisms they represent a crucial stage in animal evolu- BY AMY MAXMEN in 2009 solidified the conclusion that acoels tion — the transition some 560 million years belonged at the very base of the bilaterians3. ago from simple anemone-like organisms to crucial intermediate stage of animal evolution. That study, led by Andreas Hejnol, a devel- the zoo of complex creatures that populate the Some researchers complain that the evidence opmental biologist at the Sars International world today. is not strong enough to warrant such a dra- Centre for Marine Molecular Biology in There are about 370 species of acoel, which matic rearrangement of the evolutionary tree, Bergen, Norway, confirmed that acoels and gets its name because it lacks a coelom — the and claim that the report leaves out key data. their kin occupied an intermediate spot fluid-filled body cavity that holds the internal In any case, the vehemence of the debate shows between cnidarians and the more-complex organs in more-complex animals. Acoels also just how important these worms have become bilaterians. have just one hole for both eating and excret- in evolutionary biology. “I suddenly had the feeling that every- ing, similar to cnidarians — a group of evo- “I will say, diplomatically, this is the most thing had finally fallen into place,” says Claus lutionarily older animals containing jellyfish politically fraught paper I’ve ever written,” says Nielsen, an evolutionary biologist at the Natu- and sea anemones. But unlike the simpler cni- Max Telford, a zoologist at University College ral History Museum of Denmark, who has darians, which have only London and last author on followed acoels for 40 years as they wandered an inner and outer tissue the paper. across the tree of life. layer, acoels have a third, “THIS IS THE The debate focuses on middle tissue layer. That is MOST POLITICALLY where acoels fit in the family SHAKING THE TREE the arrangement found in tree of bilaterians, three-lay- But the study by Telford and his colleagues1 everything from scorpions FRAUGHT PAPER I’VE ered animals with bilateral has shaken the tree again and placed acoels to squids to seals, suggest- symmetry. Biologists divide within the deuterostome branches, next to the ing that acoels represent an EVER WRITTEN.” these animals into two echinoderms (which include sea urchins) and intermediate form. branches. The larger group, acorn worms. Their genetic analyses suggest That hypothesis has gained considerable sup- called protostomes, contains invertebrates that the acoels — and a marine worm named port in recent years, but a report published in such as earthworms, squids, snails and insects. Xenoturbella — descended from a more com- Nature this week1 is causing scientists to rethink The smaller group, known as deuterostomes, plex ancestor and lost many of the features seen the storyline. The study by an international includes both vertebrates and invertebrates, in other deuterostomes. team of researchers, who used new analytical such as sea urchins, humans and fish. The researchers used several approaches and techniques and data, removes acoel worms from Zoologists have generally placed acoels examined three independent data sets to come their position near the trunk of animal evolution on the earliest branch of the bilaterians — to their conclusions. First, they reanalysed data and instead places them closer to vertebrates before the split between from Hejnol’s 2009 study3, using 66 species (see ‘Competing views of animal evolution’). protostomes and deu- NATURE.COM instead of 94. Hervé Philippe, a bioinformati- The rearrangement has triggered protests terostomes — because Read Telford and cian at the University of Montreal in Quebec, from evolutionary biologists, who are alarmed the worms lack so many colleagues’ study at: Canada, and first author of the Nature paper1, that they may lose their key example of that key features such as a go.nature.com/brwepf says that the team removed species that had 1 0 F E B R U A R Y 2 0 1 1 | V O L 4 7 0 | N A T U R E | 1 6 1 © 2011 Macmillan Publishers Limited. All rights reserved NEWS FEATURE incomplete genetic data or were ‘fast-evolv- the deuterostomes. But taken together, says is their main evidence. Critics say that the ing’ — meaning that some of their genes had Telford, “the fact that our evidence points in key branches of the tree are not as statistically accumulated many changes, when compared the same direction makes me think it’s right”. strong as they should be. with genes from animal groups that emerged If acoels do fit within the deuterostomes, Because of this, Brian O’Meara, a around the same time. Phylogenetic compu- the worms must have evolved from an ances- phylogeneticist at the University of Tennessee ter programs have a well-known problem with tor with a central nervous system, a body in Knoxville, calls the new tree “suggestive, but these kinds of species and tend to group them cavity and a through-going gut that connected not definitive”. together even though they are not related. an anus and mouth — features seen in exist- The study has also come under fire for leav- Philippe and his co-workers used a more ing deuterostomes. So researchers would need ing out data that some scientists say would sophisticated mathematical model to analyse to explain how acoels and have weakened the research- sequence evolution, which helped to minimize Xenoturbella lost those and ers’ conclusions. An author this problem. Without this model and careful other characteristics. They “I’M SAD ABOUT on the paper had previously species selection, Philippe says, acoels can fall would also be left to search analysed a species of worm at the base of the animal tree. for another primitive-looking THEIR PAPER, BUT closely related to acoels After analysing sequences from nuclear lineage that represents the known as Meara stichopi, and DNA, the group made a separate evolution- evolutionary step between I’M NOT UPSET.” did not find deuterostome ary tree based on genes in mitochondria. jellyfish-like animals and microRNA. But the authors They also studied microRNAs, which regulate bilaterians. (If one even exists. Peterson says defend their decision to keep M. stichopi out gene expression but do not code for proteins. that many complex features may have emerged of their microRNA analysis owing to concerns According to co-author Kevin Peterson, a all at once.) about the quality of those data. palaeontologist at Dartmouth College in Some researchers are not ready to give up on Moreover, not everyone is convinced by Hanover, New Hampshire, microRNAs are the old ideas of where acoels fit. “I’m sad about the power of microRNA analysis, which has particularly useful for studying deep evolu- their paper, but I’m not upset,” says Hejnol. “I’d only recently been adopted for evolutionary tionary relationships. The team found that be upset if their analysis was excellent and it studies. This report marks the method’s most acoels have a type of microRNA known to be meant we lost a representative animal to bridge high-profile appearance yet as a tool to resolve specific to deuterostomes, suggesting that they an important transition in the tree of life.” relationships. Because microRNAs can be lost are related. Hejnol and his colleagues have doubts during evolution, it is possible that the deuter- The authors acknowledge that no single data about the reliability of the tree that Telford ostome microRNA in acoels originated in the set clinches the case for placing acoels within and his team built from nuclear genes, which ancestor of all bilateral animals but was later lost in the protostome line. With so much at stake, researchers are keen to resolve the issue. The US National Science Foundation has been specifically soliciting The traditional view of acoels places them at the base of the bilaterians, before the evolution of animals with a separate mouth and anus. After acoels and Xenoturbella split off, bilaterians diverged into proposals that target deep divergences in evo- protostomes and deuterostomes. lutionary history, as part of an initiative called Assembling the Tree of Life, says Tim Collins, Development of bilaterians — a programme director at the foundation. “We’ve animals with three tissue layers and bodies with symmetrical done a good job within groups, but we’ve had a left and right sides. hard time reconstructing the deepest branches of the tree of life,” he says. “These are the events that happened in a relatively short time com- pared with the amount of time that has passed since then, which makes things hard.” Last summer in Kristineberg, Sweden, Hejnol and Telford shared a room while S U I teaching a class together. They debated their L Like other bilaterians, acoels and E D Xenoturbella have three body layers differences and discussed an ongoing joint N O J but they have only one hole for . project that might settle them: sequencing the U eating and excreting.

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