Some of Earth’s first animals—including a mysterious, alien-looking creature—are spilling out of Canadian rocks

By Joshua SokolNov. 20, 2018 , 1:00 PM

KOOTENAY NATIONAL PARK IN CANADA—The drumming of the jackhammer deepens. Then, a block of shale butterflies open, exposing to crisp mountain air a surface that hasn't seen sunlight in half a billion years. "Woo!" says paleontologist Cédric Aria of the Nanjing Institute of Geology and Palaeontology in China, bracing the top slab of rock upright.

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Its underside bears charcoal-colored smudges that look vaguely like horseshoe crabs or the Millennium Falcon from Star Wars. "It's a spaceship landing area here," says expedition leader Jean-Bernard Caron, curator of invertebrate paleontology at the Royal Ontario Museum (ROM) in Toronto, Canada.

Those "spaceships" are carapaces, molted onto a long-vanished ocean floor by a species new to science. This field season they've been spilling out of the rocks here, where Caron's team has spent the past few years unearthing groundbreaking animal fossils from the Cambrian period, the coming-out party for animal life on Earth. During the Cambrian, which began about 540 million years ago, nearly all modern animal groups—as diverse as mollusks and chordates—leapt into the fossil record. Those early marine animals exhibited a dazzling array of body plans, as though evolution needed to indulge a creative streak before buckling down. For more than a century, scientists have struggled to make heads or tails—sometimes literally—of those specimens, figure out how they relate to life today, and understand what fueled the evolutionary explosion.

Com cuidado, Aria e Caron colocam a parte de cima da laje de lado. O espaço é difícil de encontrar na pedreira, empoleirado em uma saliência do tamanho de um pequeno quarto a uma altitude de 2500 metros, muito acima de Tokumm Creek. Durante anos, um local igualmente ameaçador, a cerca de 40 quilômetros a noroeste desse vale, oferecia a janela mais clara do Cambriano. Lá, em 1909, o paleontologista norte-americano Charles Doolittle Walcott descobriu o Burgess Shale, uma formação fóssil que preserva não apenas conchas duras, mas também características suaves como as pernas, os olhos e as entranhas dos creepy crawlies.

But in recent years, Caron has shown that the richest fossil-bearing rock extends many kilometers beyond Walcott's site. This summer's excavation marks his latest visit to this long Cambrian tapestry. Each new stop has offered striking views of unfamiliar animals, many already described in high-profile papers: the little fish relative Metaspriggina, a vertebrate ancestor that Caron now speculates clustered in schools; the pincered Tokummia; and the ice cream cone–shaped fossils called hyoliths, which Caron's Ph.D. student Joseph Moysiuk last year linked to shelled animals called brachiopods, some of which persist today.

Other sites around the world are also opening new vistas of the Cambrian. Scientists can now explore the animal explosion with a highlight reel of specimens, along with results from new imaging technologies and genetic and developmental studies of living organisms. "There have been a host of new discoveries," says paleontologist Doug Erwin of the Smithsonian Institution's National Museum of Natural History in Washington, D.C. Researchers may be closer than ever to fitting these strange creatures into their proper places in the tree of life—and understanding the "explosion" that birthed them.

Jean-Bernard Caron shows off the "mothership," an enigmatic Cambrian life form his team found in the Canadian Rockies this summer.

(PHOTO) JOHN LEHMANN; (FOSSIL) ROYAL ONTARIO MUSEUM

Each new find brings the simple joy of unearthing and imagining a seemingly alien creature. On a break, Caron cautiously shows off this year's crown jewel, found about a week earlier. It's an intact, hand-size carapace with a center spine, like a Prussian spiked helmet frozen in ancient rock. Another undescribed species, it seems to be related to the spaceships. Caron's team calls it the mothership.

He's nervous just holding it. Burgess Shale fossils are so valuable that Parks Canada keeps the exact locations of Caron's sites secret, monitors them with cameras, and prosecutes fossil poachers. ROM once insured a Burgess Shale specimen for half a million Canadian dollars when it went on loan, he says—and that was an animal known through multiple fossils. This is one of a kind.

"It's going to be iconic," Caron says. "It's the most extraordinary fossil I've ever found."

For years, Caron suspected Walcott's site might be rivaled elsewhere in the Rocky Mountains. The breakthrough came in 2012, near an area called Marble Canyon, where a 2003 wildfire had burned off the trees. While crossing an avalanche chute filled with broken tiles of rock, his reconnaissance party found itself surrounded by impressions of soft-bodied creatures, many with unfamiliar shapes. "It was clear that nobody had ever been walking over this pile of rocks before with this purpose in mind," says Bob Gaines, a geochemist from Pomona College in Claremont, California, who has joined Caron's expeditions since the beginning.

They returned to excavate in 2014. At least one in five of the animals they found at Marble Canyon belongs to species new to science, the team concluded. Now, they've moved on to other sites along the valley.

How Cambrian species are related to today's animals has been debated since the fossils first came to light. Walcott classified his oddities within known groups, noting that some Burgess Shale fossils, such as the brachiopods, persisted after the Cambrian or even into the present. So, for example, he concluded almost all the creatures resembling today's arthropods were crustaceans.

But later paleontologists had other ideas. Harvard University's Stephen Jay Gould perhaps best captured the charisma of Cambrian life in his 1989 book Wonderful Life: The Burgess Shale and the Nature of History, in which he lavished attention on the "weird wonders" excavated from Walcott's city block–size quarry. Gould argued that oddballs such as the aptly named Hallucigenia, a worm with legs and hard spines, seem unrelated to later animals. He slotted the unusual forms into their own phyla and argued that they were evolution's forgotten experiments, later cast aside by contingencies of fate.

Contemporary paleontologists have settled on yet another way to understand them. Consider the arthropods, arguably Earth's most successful animals. In a family tree, the spray of recent branches that end in living arthropods—spiders, insects, crustaceans—constitutes a "crown" group. But some animals in the Burgess Shale probably come from earlier "stems" that branched off before the crown arthropods. These branches of the tree don't have surviving descendants, like a childless great-uncle grinning out from a family photo. In that view, many of Gould's weird wonders are stem group organisms, related to the ancestors of current creatures although not ancestors themselves. Newer fossils from the Canadian Rockies help support that view. Caron argued in 2015, for example, that his specimens of Hallucigenia have features suggesting the animal belongs on a stem group of the velvet worms, creatures that still crawl around in tropical forests spitting slime.

All in the family

A partial schematic of a proposed family tree of arthropods shows the complex relations among living and extinct groups. Some extinct Cambrian creatures (red) may belong to "stem" groups that branched off the arthropod tree before the common ancestor of living groups like arachnids and insects.

 

(GRAPHIC) N. DESAI/SCIENCE; (DATA) JO WOLFE, MIT

Similar analysis awaits the spaceships. At first glance, Caron's team thinks they are a new species or group of radiodontans, stem arthropods that also include Anomalocaris, the Cambrian's charismatic apex predator—a clawed, fearsome-jawed swimmer half a meter long. Filling out the branches of that stem group gives a "step-by-step view of how an arthropod built its body" through evolutionary time, says paleontologist Allison Daley at the University of Lausanne in Switzerland.

Throughout much of Cambrian paleontology, that's the game—a high-stakes, sometimes contentious race to find diagnostic body parts on known or new fossils, make arguments about what taxonomic groups they belong to, and maybe revise evolutionary history in the process.

In the past few years, paleontologists have approached the problem with an array of new techniques. Those include scanning electron microscopes, which can discern a specimen's chemical makeup as well as image it, and computerized tomography (CT) scans, which can penetrate fossils without scraping away material. Those tools have also illuminated a startling series of internal features: fossilized Cambrian brains. Beginning in 2011, paleontologist Xiaoya Ma, now at the University of Exeter in the United Kingdom, published a string of papers tracing nervous tissue in exceptionally preserved Chinese fossils. Those nervous system architectures offer a parallel way to sort animals into evolutionary groups, beyond the usual anatomical structures, and other teams have presented their own compelling specimens.

In fossils of the shrimplike Chengjiangocaris kunmingensis from southwest China, for example, "we have this structure that looks almost like a pearl necklace," running almost head to tail, says Javier Ortega-Hernández, an incoming professor at Harvard. His team, led by Jie Yang at Yunnan University in Kunming, China, argued in 2016 that the necklace is a nerve cord studded with smaller clusters of neurons, themselves sprouting tiny nerve fibers. Living arthropods no longer have those fibers. But today's velvet worms and priapulid worms do, implying kinship between long-vanished stem arthropods and those groups.

Critics argue that paleontologists such as Ma and Ortega-Hernández overinterpret some fossils, spotting nervous tissues that aren't there. Many of those structures, the critics say, might just be "halos," biofilms formed when microbes broke down internal parts like muscles or guts after death. But other researchers are convinced. "If you look at the best-preserved nervous systems, there's no doubt" that the features are real, says Graham Budd, a paleontologist at Uppsala University in Sweden and an architect of the current stem-and-crown concept.

Bold claims that use anatomy to revise family trees engender similar controversy throughout the field. One argument that Hallucigenia fits with the velvet worms, for example, depends on the exact shape of its claws. But other teams counter that the claws aren't diagnostic of ancestry.
The uncertainties leave paleontologists ever hungry for newer, better specimens. "When there is a debate, you bring a new fossil and say, ‘Look, this is the feature we see,’" Caron says, warming up in a tent perched high above Tokumm Creek. "Without fossils, it's speculation."



Banff Lake Louise Bow River Columbia River Tokumm Creek Walcott Quarry Yoho National Park Yoko National Park Banff National Park Kootenay National Park 0 25 Km FRANCE FRANCE Alberta British Columbia Bilbao Madrid Marble Canyon

N. DESAI/SCIENCE

The fossils make up for the discomfort: 6 weeks in tents above the tree line warding off grizzlies with an electrified fence, contending with hot days and snow days and wildfire smoke, obeying the smelly requirement to carry everything—everything—out of the national park at the expedition's end.

It's a chilly August morning, 1 day before a helicopter comes to take all human traces away. Today is the last chance to stumble on a fossil that could crack a mystery—say, to find the body that belongs in the mothership carapace.

The nine-member team hikes from camp to their quarry, up steep, rock-littered slopes. Ridged trilobite fossils poke out from exposed layers, but on this expedition, they don't even warrant a second glance. At the quarry, most people split rock while Caron's grad students help ROM curator Maryam Akrami pack away the most recent finds in swimming-pool noodles. "It's the last day," Caron says. "No injuries!"

Each successive excavation in this valley has targeted the same band of rock, which records a single slice of geologic time. But each dig has yielded a different array of new species. That's because conditions varied across the ancient sea floor, favoring different animals. Such variation is "not a shock to anybody that has ever strapped on a snorkel and swum around," Gaines says. But this vast, wide-open valley captures that kind of diversity at a single moment, allowing glimpses of how the earliest animal ecosystems were structured.

As Caron's quarries bring this moment into ever-sharper focus, other sites have opened portals on other stages of the Cambrian. Nearly everywhere, the fossils preserve levels of squishy detail that are absent in specimens from later in Earth's fossil record. In 2012, Gaines and colleagues proposed a reason: Perhaps unique chemical conditions suffused Cambrian seas. After dead animals settled into mud on the sea floor, low levels of sulfates could have slowed decay by sulfur-loving bacteria while alkaline chemistry encased the dead animals in coats of carbonate, sealing soft tissues inside.

In summer 1984, for example, paleontologist Hou Xian-guang of Yunnan University uncovered an arthropod glistening in Cambrian mudstone, its legs seemingly alive. He had discovered the Chengjiang biota, a trove of immaculate fossils that sprawls over a region in southwest China.

Perched in their quarry 2500 meters up, paleontologists hammer open slabs of shale to expose the rare fossils inside.

JOHN LEHMANN

Slightly older than the Burgess Shale—about 518 million years old compared with the Burgess's roughly 507 million years—those deposits showcase related animals in a different style of preservation. Unlike Caron's sites, where geologic processes have squashed the fossils almost flat, the Chengjiang animals still retain some depth. Since 2015, Chinese researchers, including Hou, have capitalized on that by using CT scans to make 3D images of the specimens without destroying them. Today, three rival Chinese teams, each with international collaborators, compete to pull out new discoveries from the site. "There is an absolute landslide of material," Ortega-Hernández says.

Add to that sites such as Emu Bay in Australia, where paleontologists announced in 2011 that they had unearthed radiodontan fossils revealing their complex, multifaceted eyes; and Morocco's Fezouata Formation, which paleontologist Peter Van Roy at Ghent University in Belgium reported in 2010. Each site offers distinct insights. "Every fossil assemblage is horrifically biased," says paleontologist Nick Butterfield of the University of Cambridge in the United Kingdom, "but they're horrifically biased in different ways."

The Moroccan samples, for example, date to a little after the Cambrian, and they show a blend between the Cambrian's signature oddities and the more familiar fauna that dominated later periods. "We are still at the point of unpacking fossils," says Daley, a collaborator on that research. "This is a chance to study why some taxa go extinct and why others are able to replace them."

Although show-stopping animals keep falling out of the strata, the full significance of the Cambrian explosion remains a mystery. Arthropods, the most diverse and common creatures known from the time, littered Cambrian ecosystems. Judging by the fossils, Daley argued in a paper in May, the Cambrian witnessed both the birth and step-by-step diversification of many modern groups. Another approach yields a different answer, however. Geneticists use a tool called molecular clocks to trace back down the tree of life. By starting with genetic differences between living animals, which have accrued as a result of random mutations over the eons, molecular clocks can rewind time to the point where branches diverged.


According to recent studies using that method, modern animals began to march off into their separate phyla some 100 million years before the Cambrian. The finding implies that those groups then hung out, inconspicuous or unnoticed in the fossil record, before suddenly stepping on stage.
Paleontologists have a cryptic set of clues about life before the explosion. Long before the odd beasts of the Cambrian evolved, an even more alien set of ocean organisms left impressions on sedimentary rocks now seen in Namibia and Australia. The Ediacarans, as those fossils are called, taunt paleontologists with the same kind of interpretive challenge as the Cambrian's weird wonders. But they're even weirder. Their imprints suggest some grew in fractal patterns; others had three-part symmetry. Unhelpfully, they don't have obvious mouths, guts, or appendages. "That's where the freak flags are going now," says Jo Wolfe, a paleontologist at the Massachusetts Institute of Technology in Cambridge.

A lace crab—a long-extinct "stem" arthropod called Marrella splendens—turns up in a slab.

(PHOTO) JOHN LEHMANN; (FOSSIL) ROYAL ONTARIO MUSEUM

Most Ediacarans vanished before Cambrian deposits, perhaps perishing in the world's first mass extinction. But many researchers suspect some belong on the tree of animal life, perhaps as early stems. One Ediacaran, Kimberella, looks like an animal: a snail or slug that grazed along the sea floor. In August, Stromatoveris, a frondlike Cambrian creature already thought to be an animal, was pegged as an Ediacaran survivor on the basis of its fractal branches. That would make its Ediacaran relatives animals, too. And in September, researchers announced that an iconic Ediacaran fossil called Dickinsonia, which looks like a halved Christmas ham, contained lipid molecules that resemble those of living animals.
"We're seeing the beginning of the advent of animals in the Ediacaran," says paleobiologist Mary Droser of the University of California, Riverside. "It's more fun and exciting than just the Cambrian explosion."
And yet even as the Ediacarans shove Cambrian creatures off their perch as the first animals, Cambrian science itself continues to explode. Caron and others keep hunting for fossil features that could reveal the relationships among Ediacaran, Cambrian, and present-day groups. Other researchers struggle to explain what caused the explosion of animal forms. Atmospheric oxygen may have spiked, enabling animals to grow bigger, stronger, and more active. Or erosion could have dumped toxic calcium into the oceans, prompting organisms to shunt it into building hard skeletons.
Or biology itself could have led the way. Inventions such as predation, free swimming, and burrowing into the sea floor—all first seen in or shortly before the Cambrian—could have transformed a placid global ecology into a high-stakes contest, spurring waves of call-and-response innovation between groups. The explosion might also mark the moment when, after millions of years of quiet progress, animals had finally accrued the developmental recipes to build body parts and improvise on basic themes. That genetic toolkit, Butterfield argues, is "absolutely, astronomically, inconceivably complex. It just took a while to figure that out." Or, of course, multiple causes could have piled up together.
After a lunch break, the paleontologists chisel into a few more slabs. Gaines takes rock samples from each layer of their quarries, hoping to reconstruct each environment's chemistry. Then Caron delivers the announcement: "It's over, guys. No more digging."
The next day, its last, the ROM team breaks camp. Over several hours, a helicopter ferries nets sagging with fossils toward a staging area by the highway, making the roughly 10-minute trip again and again. Some specimens, like the spaceships, will be rushed to publication in coming months, now that visiting journalists have seen them. Other finds will sit in drawers, awaiting new techniques or the graduate student who asks the right question.
As the team huddles, waiting for its helicopter ride, tiny, rabbitlike mammals called pikas cry out from the hills. Each helicopter trip erases the signs of human presence one by one, until only carved-out quarries remain. More fossils still rest inside, pressed between folio sheets of rock, waiting for the next season.

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• Paleontology

doi:10.1126/science.aaw1202

Joshua Sokol

Joshua Sokol is a journalist based in Boston.