The Bizarre Species That Are Rewriting Animal Evolution

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Feature THE BIZARRE SPECIES THAT ARE REWRITING ANIMAL EVOLUTION Early fossils with guts, segmented bodies and other sophisticated features reveal a revolution in animal life — before the Cambrian explosion. By Traci Watson

he revolutionary animal lived and earthworms is one possibility — Yilingia is died in the muck. In its final hours, it helping to fill in key details about the evolu- inched across the sea floor, leaving tion of animals. Most importantly, Yilingia a track like a tyre print, and finally shows that some quintessential animal traits went still. Then geology set to work. had appeared half a billion years ago, earlier Over the next half a billion years, sed- than previous definitive evidence, Xiao says. iment turned to stone, preserving Yilingia is not the only creature from that the deathbed scene. The fossilized region to provide some of the earliest fossil creature looks like a piece of frayed rope meas- evidence for an important animal feature. In T 2 uring just a few centimetres wide. But it was a 2018, Xiao and his team reported on tracks trailblazer among living things. found in the Yangtze Gorges consisting of two This was the earliest-known animal to show parallel rows of dimples. The researchers pro- unequivocal evidence of two momentous pose that the trails were made by an animal innovations packaged together: the ability to from 550 million years ago that might have roam the ocean floor, and a body built from been able to burrow and had multiple pairs segments. It was also among the oldest known of appendages — which would make it one of to have clear front and back ends, and a left the earliest-known animals with legs. side that mirrored its right. Those same fea- These Chinese fossils hail from a time right Organisms named Fractofusus cover the sea floor some 560 million years ago, in a reconstruction of fossils from Newfoundland, Canada. tures are found today in animals from flies to before the Cambrian explosion, the evolution- flying foxes, from lobsters to lions. ary transformation when most of the animal The insights into the Ediacarans’ powers Palaeontologist Shuhai Xiao marvels at the groups that populate the planet today first lend support to a provocative idea: that the tracks left by this creature, Yilingia spiciformis, made their appearance in the fossil record. Sci- Cambrian explosion, that iconic evolution- and how they captured evidence of its move- entists long regarded the boundary between ary burst, was actually less revolutionary than ment. In his cluttered office at Virginia Tech the Cambrian period and the Precambrian as a many had thought. in Blacksburg, he shows off a slab of beige dividing point in evolution — a transition from The Cambrian explosion “is just another resin — a reproduction of the fossil, which was a world in which simple, strange organisms phase of evolution”, says palaeobiologist found in China’s Yangtze Gorges region and is flourished, to a time when the seas teemed Rachel Wood at the University of Edinburgh, now kept in a Chinese research institute. The with complex creatures that are the forebears UK. “It’s not a single flash event. It could not replica captures a snapshot of a moment from of nearly everything that followed. have happened without previous waves of 550 million years ago. Xiao, whose team for- But a growing number of findings reveal innovation.” mally described Yilingia last year1, traces the that the time slice just before the Cambrian, bumpy tracks it made immediately before its known as the Ediacaran (635 million to 541 mil- Tumultuous times death. “It was just moving around, and it died lion years ago), was a pivot point of animal The Ediacarans’ innovations came against a suddenly,” he says. evolution — a period that includes the earli- backdrop of planetary cataclysms. During this But that’s not the end of this creature’s story. est fossil records of anatomical innovations, time, Earth was still recovering from a long, Although nobody knows which category of such as guts and legs, and the first appearance shivery chapter when ice covered much of the life it belonged to — the group that includes of complex behaviours such as burrowing. seas. A gigantic meteor slammed into what is

CHARLOTTE G. KENCHINGTON CHARLOTTE Organisms named Fractofusus cover the sea floor some 560 million years ago, in a reconstruction of fossils from Newfoundland, Canada.

now Australia and probably kicked up enough ‘Darwin’s dilemma’ would remain unsolved about the identity of Ediacaran organisms. As dust to trigger catastrophic changes around for a century. In the 1930s and 1940s, research- more were discovered, scientists tried valiantly the globe. The planet’s very surface was split- ers found intriguing imprints in rocks in Aus- to place them on the tree of life. Some of the ting: during the Ediacaran, one supercontinent tralia and elsewhere, but those rocks were fossils were towering structures that stood broke apart and another took shape as land not definitively Precambrian. Then, several one metre tall; others resembled deflated air masses smashed together. On the continents, English schoolchildren finally gave the Edi- mattresses. They have been called lichens and no plants grew. In the ocean, oxygen levels acarans their big break in 1957. Scrambling algae, fungi and bacterial colonies. “Basically swung wildly. through a local quarry, the students noticed any interpretation you can name has been sug- Scientists once thought that complex a leaf-shaped imprint in the ancient stone. gested,” says geobiologist Lidya Tarhan at Yale life did not start until after all this tumult. Geologist Trevor Ford at the University of University in New Haven, Connecticut. In Charles Darwin’s day, no fossils had been Leicester, UK, went to see it — and recognized Finally, an audacious theory broke through found below the rock layers documenting the that it had been made by a living thing. Ford’s the welter of competing claims. In the 1980s Cambrian explosion. That blank rock record paper3 about the imprint provided definitive and 1990s, palaeontologist Adolf Seilacher troubled Darwin, who reasoned that if his the- evidence that large, complex species lived in at the University of Tübingen in Germany ory of evolution were correct, there must have the Precambrian. He ventured that the type of proposed4,5 that many Ediacaran life forms been life before the Cambrian’s riches. “The organism was probably “an algal frond”. were not animals, but instead belonged to a case at present must remain inexplicable,” he It almost certainly wasn’t. Ford’s proposal was single, bizarre group that he called the Vendo- wrote in On the Origin of Species in 1859. among the first in a long list of mistaken ideas bionta. These organisms were “an evolutionary

Feature experiment that failed” when formidable intractable imprints. Take the baffling organ- same time as the Dickinsonia specimens that predators arrived on the scene, Seilacher isms in the genus Dickinsonia. Rounded and Bobrovskiy’s team studied, or perhaps earlier7. wrote. His ideas have fallen out of favour, flat, they resembled segmented bath mats only This discovery resolves a long-standing but they challenged researchers to question a few millimetres thick, although they could Ediacaran whodunnit: what made the narrow, their assumptions. “At the time it was brilliant reach nearly 1.5 metres in length. Their strange twisting burrows that cut through Ediacaran thinking,” says geobiologist Simon Darroch at construction spawned theories that they sediments? They are among the most common Vanderbilt University in Nashville, Tennessee. were protists — a diverse group of mostly sin- Ediacaran calling cards, but are so small — only “Before that, everyone assumed they were all gle-celled organisms that includes protozoa 1.5–2 millimetres wide — that they must have jellyfish, which was even more wrong.” and some algae — or lichens, although many been created by an elusively tiny organism. Now, most scientists are reaching agree- researchers suspected that they were animals. “We never thought we’d see it,” says palae- ment that the Ediacarans were a grab bag of To try to settle the long-standing dispute, ontologist Mary Droser at the University of disparate life forms, rather than the self-con- California, Riverside. Then she got her hands tained group proposed by Seilacher. “It’s on a 3D laser scanner. inappropriate to consider them a failed Droser and her colleagues used the scanner experiment,” says palaeontologist Frances to image hundreds of tiny blobs found near the Dunn at the University of Oxford, UK. “They twisting burrows. The team’s high-resolution represent the ancestors, probably, of lots of 3D reconstructions show that the blobs were, different things.” Many scientists — although BASICALLY ANY in fact, organisms7. They were smaller than not all — are also signing up to the idea that grains of rice, but they had left–right symme- some fraction of the Ediacaran organisms were INTERPRETATION YOU try and both a front and back end, and features probably animals, including some that don’t of the burrows suggest that the creatures could look like any animal alive today. CAN NAME HAS BEEN control where they moved. Previous analysis That idea dovetails with genetic evidence SUGGESTED.” showed that some burrows wend into and that animals, or metazoans, first appeared out of the buried bodies of larger organisms, more than 600 million years ago, well before implying that Ikaria was a scavenger — the the Ediacaran. There are no definitive fossils to earliest known. Droser’s team suggests that, illustrate the dawn of the animals, but the early geobiologist Ilya Bobrovskiy, now at the to support Ikaria’s burrowing and scavenging metazoans were probably small, soft, simple California Institute of Technology in Pasa- habits, the tiny animal probably had a mouth, things, including ancestors of modern crea- dena, and his colleagues took a biochemical anus and gut. tures such as sponges and corals. Eventually, approach. Bobrovskiy used tweezers to harvest More evidence that Ediacarans had guts animals developed left–right symmetry, which thin films of organic matter — the remnants of comes from tubular organisms called cloud- is packaged with a gut, mouth and anus. Dickinsonia specimens that lived more than inids that arose around 550 million years ago. But it’s not easy to define which fossils are 550 million years ago. Analysis of the fat mol- Using high-resolution X-ray imaging to peer animals and which are not. “Would we know ecules in these biofilms showed that they were inside cloudinids’ outer tubes, researchers saw the first metazoan if we tripped over it?” Wood breakdown products of cholesterol, which is a long, cylindrical feature, which the authors wonders. “Is our search image correct?” Those found in animals’ cell membranes6. “Dickin- say is the oldest gut in the fossil record8. The questions still dog scientists. sonia was indeed an animal,” Bobrovskiy says. team found this feature in a cloudinid that Dickinsonia was a rather simple animal: it most probably belonged to the genus Saarina, Insight from imprints showed no evidence of a mouth or a gut. But and it bolsters the case that some cloudinids Although the Ediacaran fossils have bedev- earlier this year, scientists detailed what might were animals with left–right symmetry8, says illed researchers for decades, new techniques be the oldest-known animal that had both. palaeobiologist and study co-author Jim are coaxing fresh insights out of previously Called Ikaria wariootia, it lived at roughly the Schiffbauer at the University of Missouri, Columbia. The gut’s shape and other clues hint that Saarina could be an early annelid, an animal grouping that includes modern earthworms.

Alien animals New approaches are producing evidence that even the most alien-looking Ediacarans might have been animals. Take the ‘frondose’ Ediacarans, which were built from collections of miniature branches reminiscent of a fern’s lacy foliage. Some frondose organisms resembled heads of lettuce, whereas the organism Charnia masoni looked like a palm branch stuck into the sea floor. Charnia and its close relatives had a ‘pseudo-fractal’ organization like that of no living creature: the fronds were made up of branches, which were made up of sub-branches, which were made up of still- smaller branches.

Dunn and her colleagues borrowed tools IMAGES/ALAMY ZEYTUN TRAVEL Evidence indicates that Dickinsonia, an iconic organism of the Ediacaran period, was an animal. from developmental biology to understand these oddities. The researchers noted that

ZHE CHEN/NANJING INST. GEOL. PALAEONTOL.; SHUHAI XIAO/VIRGINIA TECH SHUHAI XIAO/VIRGINIA PALAEONTOL.; GEOL. INST. ZHE CHEN/NANJING A fossil from South China shows the worm-like creature Yilingia spiciformis (right) at the end of a track that it made in the sea floor.

Charnia’s fronds invariably have the same interests rather than just for themselves”, says agrees that some Ediacaran animals survived outline: widest at the bottom, smallest at the palaeobiologist Alex Liu at the University of into the Cambrian, but he argues that the big tip, with no short branches in the middle. This Cambridge, who co-wrote the paper11. picture shows a mass die-off at the boundary uniformity, a product of how the organism between the two periods. And invertebrate pal- grows, is not seen in plants or algae9. Despite Before the Big Bang aeontologist Jean-Bernard Caron at the Royal the other-worldly appearance of Charnia and As evidence mounts for Ediacaran innovation, Ontario Museum in Toronto, Canada, ques- its kin, “they’re more closely related to animals a group of researchers is using these finds to tions Wood’s tally of Ediacaran species that than they are to anything else”, Dunn says. question an icon of evolutionary history: the survived into the Cambrian. “We don’t really Researchers studying the Ediacaran have Cambrian explosion. In the past, researchers have the fossil record to support that,” he says. revealed other frondose quirks by turning often spoke of this event as the Big Bang of evo- Wood responds that although the critique is to the tools of modern ecology. One such lution — a single, supreme episode that had no fair, it’s clear that multiple Cambrian-style technique is spatial analysis, which involves prelude and suddenly changed everything. But creatures first appeared in the Ediacaran. ultra-precise mapping of a large set of organ- some researchers take the view that Ediacaran For all the contention, however, some isms that are preserved precisely where they organisms were the founders of this revolu- researchers think that answers are just around lived — information that is rarely available in tion. The burst of new species in the Cambrian the corner. Continued work on biomarkers palaeontology. But scientists have exactly “didn’t just come out of thin air”, says Wood. could pin down whether various Ediacaran such an array at their disposal in Newfound- “It must have been derived from something organisms were, in fact, animals. And palae- land, Canada, which has thousands of frondose in the Ediacaran.” ontologists are excavating new Ediacaran finds imprints. Among them are examples that date A common view holds that many Ediacaran in places such as Iran and Russia, Darroch says. back 571 million years, making them the old- organisms vanished at the Ediacaran– The latest approaches, such as spatial analysis, est-known organisms that are big enough to Cambrian boundary some 540 million hold promise too, says Xiao. These could flesh be seen without magnification. years ago. But while excavating in a remote out — at long last — what was going on in the Some of Newfoundland’s most abundant spot in Siberia, Wood and her team found oceans during the pivotal Ediacaran period. residents from around this time belong to the Cambrian-type fossils, such as animals that “I would just love to be swimming over genus Fractofusus, whose members looked lived in mineral-laden, tube-shaped shells, in these communities and see, finally, how are like mounds of fronds in the shape of an Ediacaran-age rock12. they really growing? What on Earth are they?” overturned saucer. Like its cousin Charnia, Wood and her co-authors cited these fossils Wood says. “So much would become obvious.” Fractofusus might have been an animal with in a provocative 2019 paper13, which also noted no modern analogue. Spatial analysis showed that Ediacaran animals capable of burrowing Traci Watson is Senior Editor for News and that many large Fractofusus specimens are sur- into sediments survived into the Cambrian Research Highlights at Nature in Washington DC. rounded by clusters of small ones10. “Children,” period. The ability to burrow is a hallmark of 1. Chen, Z., Zhou, C., Yuan, X. & Xiao, S. Nature 573, 412–415 says palaeobiologist Charlotte Kenchington that time, when animals dug so enthusiastically (2019). at the University of Cambridge, UK, who was that they tore up the sea floor, creating new 2. Chen, Z., Chen, X., Zhou, C., Yuan, X. & Xiao, S. Sci. Adv. a member of the team that published the ecological niches. But the Ediacarans took the 4, eaao6691 (2018). 10 3. Ford, T. D. Proc. Yorks. Geol. Soc. 31, 211–217 (1958). findings in 2015. This pattern suggests that first step, the authors say. The vaunted Cam- 4. Seilacher, A. Lethaia 22, 229–239 (1989). Fractofusus multiplied in part by shooting out brian explosion, “was simply one phase” in the 5. Seilacher, A. J. Geol. Soc. 149, 607–613 (1992). long runners on which its young developed. rise of animal diversity, they contend. 6. Bobrovskiy, I. et al. Science 361, 1246–1249 (2018). 11 7. Evans, S. D., Hughes, I. V., Gehling, J. G. & Droser, M. L. In a paper published earlier this year, sci- All of these findings tell a new story of ani- Proc. Natl Acad. Sci. USA 117, 7845–7850 (2020). entists describe long, thin, fossilized threads, mal evolution — but it is not yet clear whether 8. Schiffbauer, J. D. et al. Nature Commun. 11, 205 (2020). some stretching 4 metres, between frondose the revision will stick. Some palaeontologists 9. Dunn, F. S., Liu, A. G. & Donoghue, P. C. J. Biol. Rev. Camb. Phil. Soc. 93, 914–932 (2018). organisms in Newfoundland. These threads say that Wood’s argument, in trying to give 10. Mitchell, E. G., Kenchington, C. G., Liu, A. G., Matthews, J. J. might have been reproductive runners, the Ediacaran its due, gives short shrift to & Butterfield, N. J. Nature 524, 343–360 (2015). and could also have been used for nutrient the Cambrian explosion — which marked the 11. Liu, A. G. & Dunn, F. S. Curr. Biol. 30, 1322–1328 (2020). 12. Zhu, M., Zhuravlev, A. Yu., Wood, R. A., Zhao, F. & transport or communication. Perhaps these appearance of a vast number of creatures that Sukhov, S. S. Geology 45, 459–462 (2017). organisms were “acting in each other’s best fit clearly into modern animal groups. Xiao 13. Wood, R. et al. Nature Ecol. Evol. 3, 528–538 (2019).