TIME Magazine
December 4, 1995 Volume 146, No. 23
WHEN LIFE EXPLODED
For billions of years, simple creatures like plankton, bacteria and algae
ruled the earth. Then, suddenly, life got very complicated
BY J. MADELEINE NASH
An hour later and he might not have noticed the rock, much less stooped
to pick it up. But the early morning sunlight slanting across the Namibian
desert in southwestern Africa happened to illuminate momentarily some strange
squiggles on a chunk of sandstone. At first Douglas Erwin, a paleobiologist
at the Smithsonian Institution in Washington, wondered if the meandering
markings might be dried-up curls of prehistoric sea mud. But no, he decided
after studying the patterns for a while, these were burrows carved by a
small, wormlike creature that arose in long-vanished subtropical seas--an
archaic organism that, as Erwin later confirmed, lived about 550 million
years ago, just before the geological period known as the Cambrian.
As such, the innocuous-seeming creature and its curvy spoor mark the threshold
of a critical interlude in the history of life. For the Cambrian is a period
distinguished by the abrupt appearance of an astonishing array of multicelled
animals--animals that are the ancestors of virtually all the creatures that
now swim, fly and crawl through the visible world.
Indeed, while most people cling to the notion that evolution works its magic
over millions of years, scientists are realizing that biological change
often occurs in sudden fits and starts. And none of those fitful starts
was more dramatic, more productive or more mysterious than the one that
occurred shortly after Erwin's wormlike creature slithered through the primordial
seas. All around the world, in layers of rock just slightly younger than
that Erwin discovered, scientists have found the mineralized remains of
organisms that represent the emergence of nearly every major branch in the
zoological tree. Among them: bristle worms and roundworms, lamp shells and
mollusks, sea cucumbers and jellyfish, not to mention an endless parade
of arthropods, those spindly legged, hard-shelled ancient cousins of crabs
and lobsters, spiders and flies. There are even occasional glimpses--in
rock laid down not long after Erwin's Namibian sandstone--of small, ribbony
swimmers with a rodlike spine that are unprepossessing progenitors of the
chordate line, which leads to fish, to amphibians and eventually to humans.
Where did this extraordinary bestiary come from, and why did it emerge so
quickly? In recent years, no question has stirred the imagination of more
evolutionary experts, spawned more novel theories or spurred more far-flung
expeditions. Life has occupied the planet for nearly 4 billion of its 4.5
billion years. But until about 600 million years ago, there were no organisms
more complex than bacteria, multicelled algae and single-celled plankton.
The first hint of biological ferment was a plethora of mysterious palm-shape,
frondlike creatures that vanished as inexplicably as they appeared. Then,
543 million years ago, in the early Cambrian, within the span of no more
than 10 million years, creatures with teeth and tentacles and claws and
jaws materialized with the suddenness of apparitions. In a burst of creativity
like nothing before or since, nature appears to have sketched out the blueprints
for virtually the whole of the animal kingdom. This explosion of biological
diversity is described by scientists as biology's Big Bang.
Over the decades, evolutionary theorists beginning with Charles Darwin have
tried to argue that the appearance of multicelled animals during the Cambrian
merely seemed sudden, and in fact had been preceded by a lengthy period
of evolution for which the geological record was missing. But this explanation,
while it patched over a hole in an otherwise masterly theory, now seems
increasingly unsatisfactory. Since 1987, discoveries of major fossil beds
in Greenland, in China, in Siberia, and now in Namibia have shown that the
period of biological innovation occurred at virtually the same instant in
geologic time all around the world.
What could possibly have powered such a radical advance? Was it something
in the organisms themselves or the environment in which they lived? Today
an unprecedented effort to answer these questions is under way. Geologists
and geochemists are reconstructing the Precambrian planet, looking for changes
in the atmosphere and ocean that might have put evolution into sudden overdrive.
Developmental biologists are teasing apart the genetic toolbox needed to
assemble animals as disparate as worms and flies, mice and fish. And paleontologists
are exploring deeper reaches of the fossil record, searching for organisms
that might have primed the evolutionary pump. "We're getting data,"
says Harvard University paleontologist Andrew Knoll, "almost faster
than we can digest it."
Every few weeks, it seems, a new piece of the puzzle falls into place. Just
last month, in an article published by the journal Nature, an international
team of scientists reported finding the exquisitely preserved remains of
a 1-in.- to 2-in.-long animal that flourished in the Cambrian oceans 525
million years ago. From its flexible but sturdy spinal rod, the scientists
deduced that this animal--dubbed Yunnanozoon lividum, after the Chinese
province in which it was found--was a primitive chordate, the oldest ancestor
yet discovered of the vertebrate branch of the animal kingdom, which includes
Homo sapiens.
Even more tantalizing, paleontologists are gleaning insights into the enigmatic
years that immediately preceded the Cambrian explosion. Until last spring,
when John Grotzinger, a sedimentologist from M.I.T., led Erwin and two dozen
other scientists on an expedition to the Namibian desert, this fateful period
was obscured by a 20 million--year gap in the fossil record. But with the
find in Namibia, as Grotzinger and three colleagues reported in the Oct.
27 issue of Science, the gap suddenly filled with complex life. In layer
after layer of late Precambrian rock, heaved up in the rugged outcroppings
the Namibians call kopfs (after the German word for "head"), Grotzinger's
team has documented the existence of a flourishing biological community
on the cusp of a startling transformation, a community in which small wormlike
somethings, small shelly somethings--perhaps even large frondlike somethings--were
in the process of crossing over a shadow line into uninhabited ecospace.
Here, then, are highlights from the tale that scientists are piecing together
of a unique and dynamic time in the history of the earth, when continents
were rifting apart, genetic programs were in flux, and tiny organisms in
vast oceans dreamed of growing large.
THE WEIRD WONDERS
Inside locked cabinets at the Smithsonian Institution nestle snapshots in
stone as vivid as any photograph. There, engraved on slices of ink-black
shale, are the myriad inhabitants of a vanished world, from plump Aysheaia
prancing on caterpillar-like legs to crafty Ottoia, lurking in a burrow
and extending its predatory proboscis. Excavated in the early 1900s from
a geological formation in the Canadian Rockies known as the Burgess Shale,
these relics of the earliest animals to appear on earth are now revered
as priceless treasures. Yet for half a century after their discovery, the
Burgess Shale fossils attracted little scientific attention as researchers
concentrated on creatures that were larger and easier to understand--like
the dinosaurs that roamed the earth nearly 300 million years later.
Then, starting in the late 1960s, three paleontologists--Harry Whittington
of the University of Cambridge in England and his two students, Derek Briggs
and Simon Conway Morris--embarked on a methodical re-examination of the
Burgess Shale fossils. Under bright lights and powerful microscopes, they
coaxed fine-grain anatomical detail from the shale's stony secrets: the
remains of small but substantial animals that were overtaken by a roaring
underwater mudslide 515 million years ago and swept into water so deep and
oxygen-free that the bacteria that should have decayed their tissues couldn't
survive. Preserved were not just the hard-shelled creatures familiar to
Darwin and his contemporaries but also the fossilized remains of soft-bodied
beasts like Aysheaia and Ottoia. More astonishing still were remnants of
delicate interior structures, like Ottoia's gut with its last, partly digested
meal.
Soon, inspired reconstructions of the Cambrian bestiary began to create
a stir at paleontological gatherings. Startled laughter greeted the unveiling
of oddball Opabinia, with its five eyes and fire-hose-like proboscis. Credibility
was strained by Hallucigenia, when Conway Morris depicted it as dancing
along on needle-sharp legs, and also by Wiwaxia, a whimsical armored slug
with two rows of upright scales. And then there was Anomalocaris, a fearsome
predator that caught its victims with spiny appendages and crushed them
between jaws that closed like the shutter of a camera. "Weird wonders,"
Harvard University paleontologist Stephen Jay Gould called them in his 1989
book, Wonderful Life, which celebrated the strangeness of the Burgess Shale
animals.
But even as Wonderful Life was being published, the discovery of new Cambrian-era
fossil beds in Sirius Passet, Greenland, and Yunnan, China, was stripping
some of the weirdness from the wonders. Hallucigenia's impossibly pointed
legs, for example, were unmasked as the upside-down spines of a prehistoric
velvet worm. In similar fashion, Wiwaxia, some scientists think, is probably
allied with living bristle worms. And the anomalocaridids--whose variety
is rapidly expanding with further research--appear to be cousins, if not
sisters, of the amazingly diverse arthropods.
The real marvel, says Conway Morris, is how familiar so many of these animals
seem. For it was during the Cambrian (and perhaps only during the Cambrian)
that nature invented the animal body plans that define the broad biological
groupings known as phyla, which encompass everything from classes and orders
to families, genera and species. For example, the chordate phylum includes
mammals, birds and fish. The class Mammalia, in turn, covers the primate
order, the hominid family, the genus Homo and our own species, Homo sapiens.
EVOLVING AT SUPERSONIC SPEED
Scientists used to think that the evolution of phyla took place over a period
of 75 million years, and even that seemed impossibly short. Then two years
ago, a group of researchers led by Grotzinger, Samuel Bowring from M.I.T.
and Harvard's Knoll took this long-standing problem and escalated it into
a crisis. First they recalibrated the geological clock, chopping the Cambrian
period to about half its former length. Then they announced that the interval
of major evolutionary innovation did not span the entire 30 million years,
but rather was concentrated in the first third. "Fast," Harvard's
Gould observes, "is now a lot faster than we thought, and that's extraordinarily
interesting."
What Knoll, Grotzinger and colleagues had done was travel to a remote region
of northeastern Siberia where millenniums of relentless erosion had uncovered
a dramatic ledger of rock more than half a mile thick. In ancient seabeds
near the mouth of the Lena River, they spotted numerous small, shelly fossils
characteristic of the early Cambrian. Even better, they found cobbles of
volcanic ash containing minuscule crystals of a mineral known as zircon,
possibly the most sensitive timepiece nature has yet invented.
Zircon dating, which calculates a fossil's age by measuring the relative
amounts of uranium and lead within the crystals, had been whittling away
at the Cambrian for some time. By 1990, for example, new dates obtained
from early Cambrian sites around the world were telescoping the start of
biology's Big Bang from 600 million years ago to less than 560 million years
ago. Now, with information based on the lead content of zircons from Siberia,
virtually everyone agrees that the Cambrian started almost exactly 543 million
years ago and, even more startling, that all but one of the phyla in the
fossil record appeared within the first 5 million to 10 million years. "We
now know how fast fast is," grins Bowring. "And what I like to
ask my biologist friends is, How fast can evolution get before they start
feeling uncomfortable?"
FREAKS OR ANCESTORS?
The key to the Cambrian explosion, researchers are now convinced, lies in
the Vendian, the geological period that immediately preceded it. But because
of the frustrating gap in the fossil record, efforts to explore this critical
time interval have been hampered. For this reason, no one knows quite what
to make of the singular frond-shape organisms that appeared tens of millions
of years before the beginning of the Cambrian, then seemingly died out.
Are these puzzling life-forms--which Yale University paleobiologist Adolf
Seilacher dubbed the "vendobionts"--linked somehow to the creatures
that appeared later on, or do they represent a totally separate chapter
in the history of life?
Seilacher has energetically championed the latter explanation, speculating
that the vendobionts represent a radically different architectural solution
to the problem of growing large. These "creatures"--which reached
an adult size of 3 ft. or more across--did not divide their bodies into
cells, believes Seilacher, but into compartments so plumped with protoplasm
that they resembled air mattresses. They appear to have had no predators,
says Seilacher, and led a placid existence on the ocean floor, absorbing
nutrients from seawater or manufacturing them with the help of symbiotic
bacteria.
UCLA paleontologist Bruce Runnegar, however, disagrees with Seilacher. Runnegar
argues that the fossil known as Ernietta, which resembles a pouch made of
wide-wale corduroy, may be some sort of seaweed that generated food through
photosynthesis. Charniodiscus, a frond with a disklike base, he classifies
as a colonial cnidarian, the phylum that includes jellyfish, sea anemones
and sea pens. And Dickinsonia, which appears to have a clearly segmented
body, Runnegar tentatively places in an ancestral group that later gave
rise to roundworms and arthropods. The Cambrian explosion did not erupt
out of the blue, argues Runnegar. "It's the continuation of a process
that began long before."
The debate between Runnegar and Seilacher is about to get even more heated.
For, as pictures that accompany the Science article reveal, researchers
have returned from Namibia with hard evidence that a diverse community of
organisms flourished in the oceans at the end of the Vendian, just before
nature was gripped by creative frenzy. Runnegar, for instance, is currently
studying the fossil of a puzzling conical creature that appears to be an
early sponge. M.I.T.'s Beverly Saylor is sorting through sandstones that
contain a menagerie of small, shelly things, some shaped like wine goblets,
others like miniature curtain rods. And Guy Narbonne of Queen's University
in Ontario, Canada, is trying to make sense of Dickinsonia-like creatures
found just beneath the layer of rock where the Cambrian officially begins.
What used to be a gap in the fossil record has turned out to be teeming
with life, and this single, stunning insight into late-Precambrian ecology,
believes Grotzinger, is bound to reframe the old argument over the vendobionts.
For whether they are animal ancestors or evolutionary dead ends, says Grotzinger,
Dickinsonia and its cousins can no longer be thought of as sideshow freaks.
Along with the multitudes of small, shelly organisms and enigmatic burrowers
that riddled the sea floor with tunnels and trails, the vendobionts have
emerged as important clues to the Cambrian explosion. "We now know,"
says Grotzinger, "that evolution did not proceed in two unrelated pulses
but in two pulses that beat together as one."
BREAKING THROUGH THE ALGAE
To human eyes, the world on the eve of the Cambrian explosion would have
seemed an exceedingly hostile place. Tectonic forces unleashed huge earthquakes
that broke continental land masses apart, then slammed them back together.
Mountains the size of the Himalayas shot skyward, hurling avalanches of
rock, sand and mud down their flanks. The climate was in turmoil. Great
ice ages came and went as the chemistry of the atmosphere and oceans endured
some of the most spectacular shifts in the planet's history. And in one
way or another, says Knoll, these dramatic upheavals helped midwife complex
animal life by infusing the primordial oceans with oxygen.
Without oxygen to aerate tissues and make vital structural components like
collagen, notes Knoll, animals simply cannot grow large. But for most of
earth's history, the production of oxygen through photosynthesis--the metabolic
alchemy that allowed primordial algae to turn carbon dioxide, water and
sunlight into energy-- was almost perfectly balanced by oxygen-depleting
processes, especially organic decay. Indeed, the vast populations of algae
that smothered the Precambrian oceans generated tons of vegetative debris,
and as bacteria decomposed this slimy detritus, they performed photosynthesis
in reverse, consuming oxygen and releasing carbon dioxide, the greenhouse
gas that traps heat and helps warm the planet.
For oxygen to rise, then, the planet's burden of decaying organic matter
had to decline. And around 600 million years ago, that appears to be what
happened. The change is reflected in the chemical composition of rocks like
limestone, which incorporate two isotopes of carbon in proportion to their
abundance in seawater--carbon 12, which is preferentially taken up by algae
during photosynthesis, and carbon 13, its slightly heavier cousin. By sampling
ancient limestones, Knoll and his colleagues have determined that the ratio
of carbon 12 to carbon 13 remained stable for most of the Proterozoic Eon,
a boggling expanse of time that stretched from 2.5 billion years ago to
the end of the Vendian. But at the close of the Proterozoic, just prior
to the Cambrian explosion, they pick up a dramatic rise in carbon 13 levels,
suggesting that carbon 12 in the form of organic material was being removed
from the oceans.
One mechanism, speculates Knoll, could have been erosion from steep mountain
slopes. Over time, he notes, tons of sediment and rock that poured into
the sea could have buried algal remains that fell to the sea floor. In addition,
he says, rifting continents very likely changed the geometry of ocean basins
so that water could not circulate as vigorously as before. The organic carbon
that fell to the sea floor, then, would have stayed there, never cycling
back to the ocean surface and into the atmosphere. As levels of atmospheric
carbon dioxide dropped, the earth would have cooled. Sure enough, says Knoll,
a major ice age ensued around 600 million years ago--yet another link in
a complex chain that connects geological and geochemical events to a momentous
advance in biology.
Biology also influenced geochemistry, says Indiana University biochemist
John Hayes. In fact, in a paper published in Nature earlier this year, Hayes
and his colleagues argue that guts, those simple conduits that take food
in at one end and expel wastes at the other, may be the key to the Cambrian
explosion. Their reasoning goes something like this: animals grazed on the
algae, packaging the leftover organic material into fecal pellets. These
pellets dropped to the ocean depths, depriving oxygen-depleting bacteria
of their principal food source. The evidence? Organic lipids in ancient
rocks, notes Hayes, underwent a striking change in carbon-isotope ratios
around 550 million years ago. Again, the change suggests that food sources
rich in carbon 12, like algae, were being "express mailed" to
the ocean floor.
THE GENETIC TOOL KIT
The animals that aerated the precambrian oceans could have resembled the
wormlike something that left its meandering marks on the rock Erwin lugged
back from Namibia. More advanced than a flatworm, which was not rigid enough
to burrow through sand, this creature would have had a sturdy, fluid-filled
body cavity. It would have had musculature capable of strong contractions.
It probably had a heart, a well-defined head with an eye for sensing light
and, last but not least, a gastrointestinal tract with an opening at each
end. What kind of genetic machinery, Erwin wondered, did nature need in
order to patch together such a creature?
Over the summer, Erwin pondered this problem with two paleontologist friends,
David Jablonski of the University of Chicago and James Valentine of the
University of California, Berkeley. Primitive multicelled organisms like
jellyfish, they reasoned, have three so-called homeotic homeobox genes,
or Hox genes, which serve as the master controllers of embryonic development.
Flatworms have four, arthropods like fruit flies have eight, and the primitive
chordate Branchiostoma (formerly known as Amphioxus) has 10. So around 550
million years ago, Erwin and the others believe, some wormlike creature
expanded its Hox cluster, bringing the number of genes up to six. Then,
"Boom!" shouts Jablonski. "At that point, perhaps, life crossed
some sort of critical threshold." Result: the Cambrian explosion.
The proliferation of wildly varying body plans during the Cambrian, scientists
reason, therefore must have something to do with Hox genes. But what? To
find out, developmental biologist Sean Carroll's lab on the University of
Wisconsin's Madison campus has begun importing tiny velvet worms that inhabit
rotting logs in the dry forests of Australia. Blowing bubbles of spittle
and waving their fat legs in the air, they look, he marvels, virtually identical
to their Cambrian cousin Aysheaia, whose evocative portrait appears in the
pages of the Burgess Shale. Soon Carroll hopes to answer a pivotal question:
Is the genetic tool kit needed to construct a velvet worm smaller than the
one the arthropods use? Already Carroll suspects that the Cambrian explosion
was powered by more than a simple expansion in the number of Hox genes.
Far more important, he believes, were changes in the vast regulatory networks
that link each Hox gene to hundreds of other genes. Think of these genes,
suggests Carroll, as the chips that run a computer. The Cambrian explosion,
then, may mark not the invention of new hardware, but rather the elaboration
of new software that allowed existing genes to perform new tricks. Unusual-looking
arthropods, for example, might be cobbled together through variations of
the genetic software that codes for legs. "Arthropods," observes
paleoentomologist Jarmila Kukalova-Peck of Canada's Carleton University,
"are all legs"--including the "legs" that evolved into
jaws, claws and even sex organs.
BEYOND DARWINISM
Of course, understanding what made the Cambrian explosion possible doesn't
address the larger question of what made it happen so fast. Here scientists
delicately slide across data-thin ice, suggesting scenarios that are based
on intuition rather than solid evidence. One favorite is the so-called empty
barrel, or open spaces, hypothesis, which compares the Cambrian organisms
to homesteaders on the prairies. The biosphere in which the Cambrian explosion
occurred, in other words, was like the American West, a huge tract of vacant
property that suddenly opened up for settlement. After the initial land
rush subsided, it became more and more difficult for naive newcomers to
establish footholds.
Predation is another popular explanation. Once multicelled grazers appeared,
say paleontologists, it was only a matter of time before multicelled predators
evolved to eat them. And, right on cue, the first signs of predation appear
in the fossil record exactly at the transition between the Vendian and the
Cambrian, in the form of bore holes drilled through shelly organisms that
resemble stacks of miniature ice-cream cones. Seilacher, among others, speculates
that the appearance of protective shells and hard, sharp parts in the late
Precambrian signaled the start of a biological arms race that did in the
poor, defenseless vendobionts.
Even more speculative are scientists' attempts to address the flip side
of the Cambrian mystery: why this evolutionary burst, so stunning in speed
and scope, has never been equaled. With just one possible exception--the
Bryozoa, whose first traces turn up shortly after the Cambrian--there is
no record of new phyla emerging later on, not even in the wake of the mass
extinction that occurred 250 million years ago, at the end of the Permian
period.
Why no new phyla? Some scientists suggest that the evolutionary barrel still
contained plenty of organisms that could quickly diversify and fill all
available ecological niches. Others, however, believe that in the surviving
organisms, the genetic software that controls early development had become
too inflexible to create new life-forms after the Permian extinction. The
intricate networks of developmental genes were not so rigid as to forbid
elaborate tinkering with details; otherwise, marvels like winged flight
and the human brain could never have arisen. But very early on, some developmental
biologists believe, the linkages between multiple genes made it difficult
to change important features without lethal effect. "There must be
limits to change," says Indiana University developmental biologist
Rudolf Raff. "After all, we've had these same old body plans for half
a billion years."
The more scientists struggle to explain the Cambrian explosion, the more
singular it seems. And just as the peculiar behavior of light forced physicists
to conclude that Newton's laws were incomplete, so the Cambrian explosion
has caused experts to wonder if the twin Darwinian imperatives of genetic
variation and natural selection provide an adequate framework for understanding
evolution. "What Darwin described in the Origin of Species," observes
Queen's University paleontologist Narbonne, "was the steady background
kind of evolution. But there also seems to be a non-Darwinian kind of evolution
that functions over extremely short time periods--and that's where all the
action is."
In a new book, At Home in the Universe (Oxford University Press; $25), theoretical
biologist Stuart Kauffman of the Santa Fe Institute argues that underlying
the creative commotion during the Cambrian are laws that we have only dimly
glimpsed--laws that govern not just biological evolution but also the evolution
of physical, chemical and technological systems. The fanciful animals that
first appeared on nature's sketchpad remind Kauffman of early bicycles,
with their odd-size wheels and strangely angled handlebars. "Soon after
a major innovation," he writes, "discovery of profoundly different
variations is easy. Later innovation is limited to modest improvements on
increasingly optimized designs."
Biological evolution, says Kauffman, is just one example of a self-organizing
system that teeter-totters on the knife edge between order and chaos, "a
grand compromise between structure and surprise." Too much order makes
change impossible; too much chaos and there can be no continuity. But since
balancing acts are necessarily precarious, even the most adroit tightrope
walkers sometimes make one move too many. Mass extinctions, chaos theory
suggests, do not require comets or volcanoes to trigger them. They arise
naturally from the intrinsic instability of the evolving system, and superior
fitness provides no safety net.
In fact, some of prehistory's worst mass extinctions took place during the
Cambrian itself, and they probably occurred for no obvious reason. Rather,
just as the tiniest touch can cause a steeply angled sand pile to slide,
so may a small evolutionary advance that gives one species a temporary advantage
over another be enough to bring down an entire ecosystem. "These patterns
of speciations and extinctions, avalanching across ecosystems and time,"
warns Kauffman, are to be found in every chaotic system--human and biological.
"We are all part of the same pageant," as he puts it. Thus, even
in this technological age, we may have more in common than we care to believe
with the weird--and ultimately doomed--wonders that radiated so hopefully
out of the Cambrian explosion.
Copyright 1995 Time Inc. All rights reserved.