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A HISTORY OF ANIMALS

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Beginnings

The Earth is about 4.5 billion years old, and life itself began perhaps 3.8 billion years ago or so. Animals arrived much later – perhaps a billion years ago, but probably some time after that. For most of the Earth’s history, then, there was life, but no animals. What we had, over vast stretches of time, was a world of single-celled organisms in the sea. Much of life today goes on in exactly that form.

When picturing this long era before animals, one might start by visualizing single-celled organisms as solitary beings: countless tiny islands, doing nothing more than floating about, taking in food (somehow), and dividing into two. But single-celled life is, and probably was, far more entangled than that; many of these organisms live in association with others, sometimes in mere truce and coexistence, sometimes in genuine collaboration. Some of the early collaborations were probably so tight that they were really a departure from a “single-celled” mode of life, but they were not organized in anything like the way that our animal bodies are organized.

When picturing this world, we might also presume that because there are no animals, there’s no behavior, and no sensing of the world outside. Again, not so. Single-celled organisms can sense and react. Much of what they do counts as behavior only in a very broad sense, but they can control how they move and what chemicals they make, in response to what they detect going on around them. In order for any organism to do this, one part of it must be receptive, able to see or smell or hear, and another part must be active, able to make something useful happen. The organism must also establish a connection of some sort, an arc, between these two parts.

One of the best-studied systems of this kind is seen in the familiar E. coli bacteria, which live in vast numbers inside and around us. E. coli has a sense of taste, or smell; it can detect welcome and unwelcome chemicals around it, and it can react by moving toward concentrations of some chemicals and away from others. The exterior of each E. coli cell has an array of sensors – collections of molecules bridging the cell’s outer membrane. That’s the “input” part of the system. The “output” part is composed of flagella, the long filaments with which the cell swims. An E. coli bacterium has two main motions: it can run or tumble. When it runs, it moves in a straight line, and when it tumbles, as you might expect, it randomly changes direction. A cell continually switches between these two activities, but if it detects an increasing concentration of food, its tumbling is reduced.

A bacterium is so small that its sensors alone can give it no indication of the direction that a good or bad chemical is coming from. To overcome this problem, the bacterium uses time to help it deal with space. The cell is not interested in how much of a chemical is present at any given moment, but rather in whether that concentration is increasing or decreasing. After all, if the cell swam in a straight line simply because the concentration of a desirable chemical was high, it might travel away from chemical nirvana, not toward it, depending on the direction it’s pointing. The bacterium solves this problem in an ingenious manner: as it senses its world, one mechanism registers what conditions are like right now, and another records how things were a few moments ago. The bacterium will swim in a straight line as long as the chemicals it senses seem better now than those it sensed a moment ago. If not, it’s preferable to change course.

Bacteria are one among several kinds of single-celled life, and they are simpler in many ways than the cells that eventually came together to make animals. Those cells, eukaryotes, are larger and have an elaborate internal structure. Arising perhaps 1.5 billion years ago, they are the descendants of a process in which one small bacterium-like cell swallowed another. Single-celled eukaryotes, in many cases, have more complicated capacities to taste and swim, and they also edge close to a particularly important sense: vision.

Light, for living things, has a dual role. For many it is an intrinsically important resource, a source of energy. It can also be a source of information, an indicator of other things. This second use, so familiar to us, is not easily achieved by a tiny organism. Much of the use of light by single-celled organisms is for solar power; like plants, they sunbathe. Various bacteria can sense light and respond to its presence. Organisms so small have a difficult time determining the direction light is coming from, let alone focusing an image, but a range of single-celled eukaryotes, and perhaps a few remarkable bacteria, do have the beginnings of seeing. The eukaryotes have “eyespots,” patches that are sensitive to light, connected to something that shades or focuses the incoming light, making it more informative. Some eukaryotes seek light, some avoid it, and some switch between the two; they follow light when they want to take in energy, and avoid it when their energy supplies are full. Others seek out light when it is not too strong and avoid it when the intensity becomes dangerous. In all these cases, there is a control system connecting the eyespot with a mechanism that enables the cell to swim.

Much of the sensing done by these tiny organisms is aimed at finding food and avoiding toxins. Even in the earliest work on E. coli, though, it seemed that something else was going on. They were also attracted to chemicals they could not eat. Biologists who work on these organisms are more and more inclined to see the senses of bacteria as attuned to the presence and activities of other cells around them, not just to washes of edible and inedible chemicals. The receptors on the surfaces of bacterial cells are sensitive to many things, and these include chemicals that bacteria themselves tend to excrete for various reasons – sometimes just as overflow of metabolic processes. This may not sound like much, but it opens an important door. Once the same chemicals are being sensed and produced, there is the possibility of coordination between cells. We have reached the birth of social behavior.

An example is quorum sensing. If a chemical is both produced and sensed by a particular kind of bacterium, it can be used by those bacteria to assess how many individuals of the same kind are around. By doing this, they can work out whether enough bacteria are nearby for it to be worthwhile to produce a chemical that does its job only if many cells make it at once.

An early case of quorum sensing to be uncovered involves – appropriately for this book – the sea and a cephalopod. Bacteria living inside a Hawaiian squid produce light by a chemical reaction, but only if enough other bacteria are around to join in. The bacteria control their illumination by detecting the local concentration of an “inducer” molecule, which is made by the bacteria and gives each individual a sense of how many potential light producers are around. As well as lighting up, the bacteria follow the rule that the more of this chemical you sense, the more you make.

When enough light is being produced, the squid who house the bacteria gain the benefit of camouflage. This is because they hunt at night, when moonlight would normally cast their body’s shadow down to predators below. Their internal lights cancel the shadow. Meanwhile, the bacteria seem to benefit from the hospitable living quarters provided by the squid.

This aquatic setting is the right one to have in mind when thinking about these early stages in life’s history – though in the evolutionary story we are at a point long before there were any squid. The chemistry of life is an aquatic chemistry. We can get by on land only by carrying a huge amount of salt water around with us. And many of the evolutionary moves made at these early stages – those giving birth to sensing, behavior, and coordination – would have depended on the sea’s free movement of chemicals.

So far, all the cells we’ve met are sensitive to external conditions. Some also have a special sensitivity to other organisms, including organisms of the same kind. Within that category, some cells show a sensitivity to chemicals that other organisms make to be perceived, as opposed to chemicals made as mere byproducts. That last category – chemicals that are made because they’ll be perceived and responded to by others – brings us to the threshold of signaling and communication.

We’re arriving at two thresholds, though, not one. In a world of single-celled aquatic life, we’ve seen how individuals can sense their surroundings and signal to others. But we’re about to look at the transition from single-celled life to many-celled life. Once that transition is under way, the signaling and sensing that connected one organism to another become the basis of new interactions which take place within the new forms of life now emerging. Sensing and signaling between organisms gives rise to sensing and signaling within an organism. A cell’s means for sensing the external environment become a means to sense what other cells within the same organism are up to, and what they might be saying. A cell’s “environment” is largely made up of other cells, and the viability of the new, larger organism will depend on coordination between these parts.

~ Living Together

Animals are multicellular; we contain many cells that act in concert. The evolution of animals began when some cells submerged their individuality, becoming parts of large joint ventures. The transition to a multicellular form of life occurred many times, leading once to animals, once to plants, on other occasions to fungi, various seaweeds, and less conspicuous organisms. Most likely, the origin of animals did not stem from a meeting between lone cells who drifted together. Rather, animals arose from a cell whose daughters did not separate properly during cell division. Usually, when a single-celled organism divides into two, the daughters go their separate ways, but not always. Imagine a ball of cells that forms when one cell divides and the results stay together – and the process repeats several times. The cells in the clump probably ate bacteria as they hovered together in the sea.

The next stages in the history are unclear; a couple of rival scenarios are on the table, based on different kinds of evidence. In one scenario, perhaps the majority view, some of these balls of cells forsook their suspended life and settled on the sea floor. There they began feeding by filtering water through channels in their bodies; the result was the evolution of the sponge.

A sponge? It seems that one could hardly pick a more implausible ancestor: sponges, after all, do not move. They look like an immediate dead end. However, only the adult sponge is stationary. The babies, or larvae, are another matter. They are often swimmers, who search for a place to settle and become an adult sponge. Sponge larvae have no brains, but they have sensors on their bodies sniffing their world. Perhaps some of these larvae opted to keep swimming, rather than settle down. They remained mobile, became sexually mature while suspended in the water, and began a new kind of life. They became the mothers of all the other animals, leaving their relatives fixed to the sea floor.

The scenario I just described is motivated by the view that sponges are the living animals most distantly related to us. Distant does not mean old; present-day sponges are the products of as much evolution as we are. But for various reasons, if sponges did branch off very early, they are thought to offer clues to what the earliest animals were like. Recent work, however, suggests that sponges might not, after all, be the animals most distantly related to us; instead, this title may belong to the comb jellies.

A comb jelly, or ctenophore, looks like a very delicate jellyfish. It’s an almost transparent globe, with colorful bands of hair-like strands running down its body. Comb jellies have often been seen as cousins of jellyfish, but the observable similarities might be misleading; they might have split off from the line leading to other animals even before sponges did. If this is true, it does not mean that our ancestor looked like a present-day comb jelly. But the comb jelly scenario does motivate a different picture of the early evolutionary stages. Again we start with a clump of cells, but then imagine that this clump folds into a filmy globe-like form, and swims in a simple rhythm as it lives suspended in the water column. The evolution of animals proceeds from there – from a hovering ghost-like mother, rather than a wriggling sponge larva who refused to settle down.

When multicellular organisms arise, the cells that were once organisms in their own right begin to work as parts of larger units. If the new organism is to be any more than a clump of cells glued together, it requires coordination. Earlier I described the forms of sensing and acting seen in single-celled life. In multicellular organisms, these sensory and behavioral systems become more complicated. Further, the very existence of these new entities – animal bodies – depends on those capacities for sensing and action. Sensing and signaling between organisms gives rise to sensing and signaling within them. The “behavioral” capacities of cells that once lived as whole organisms become the basis for coordination within the new multicellular organism.

Animals give that coordination several roles. One role is seen also in other multicellular organisms, such as plants: signaling between cells is used to build the organism, to bring it into being. Another role exists on a faster time scale, and is especially characteristic of animal life. In all but a few animals, the chemical interactions between some cells become the basis for a nervous system, small or large. And in some of these animals, a mass of such cells concentrated together, sparking in a chemo-electrical storm of repurposed signaling, become a brain.

~ Neurons and Nervous Systems

A nervous system is made of many parts, but the most significant are the unusually shaped cells called neurons. Their long strands and elaborate branchings form a maze through our heads and bodies.

The activity of neurons depends on two things. One is their electrical excitability, seen especially in the action potential, an electrical spasm that moves along a cell in a chain reaction. The other is chemical sensing and signaling. A neuron will release a tiny spray of chemicals into the gap or “cleft” between it and another neuron. These chemicals, when they are detected at the other side, can help trigger (or in some cases suppress) an action potential in that adjoining cell. This chemical influence is the residue of ancient signaling between organisms, pressed inward. The action potential, too, existed in cells before animals evolved, and exists today outside them. The first one ever measured, in fact, was in a plant, the Venus flytrap, at the instigation of Charles Darwin in the nineteenth century. Even some single-celled organisms have action potentials.

What nervous systems make possible is not cell-to-cell signaling itself – that is common – but particular kinds of signaling. Nervous systems are fast, first of all. Except in a few cases like the Venus flytrap, plants act on a slower time scale. Second, the neuron’s long, tenuous projections enable one cell to reach some distance through the brain or body and affect just a few distant cells; influence is targeted. Evolution has transformed cell-to-cell signaling from an activity in which cells simply broadcast their signals to whoever is close enough and listening into something different: an organized network. In a nervous system like our own, the result is a continual electrical clamor, a symphony of tiny cellular fits, mediated by sprays of chemicals across the gaps where one cell reaches out to another.

This internal tumult is also expensive. Neurons cost a great deal of energy to run and maintain. Creating their electrical spasms is like the continual charging and discharging of a battery, hundreds of times each second. In an animal like us, a large proportion of the energy taken in as food, nearly a quarter in our case, is spent just keeping the brain running. Any nervous system is a very costly machine. Soon I’ll turn to the history of this machine, when it might have evolved and how. First, I’ll spend some time on a general question about why.

Why is it worth having such a brain, or any nervous system? What are they for? As I see it, two pictures guide people’s thinking about the matter. These pictures are visible in scientific work and they permeate philosophy, too; their roots run deep. According to the first view, the original and fundamental function of the nervous system is to link perception with action. Brains are for the guidance of action, and the only way to “guide” action in a useful way is to link what is done to what is seen (and touched, and tasted). The senses track what’s going on in the environment, and nervous systems use this information to work out what to do. I’ll call this the sensory-motor view of nervous systems and their function.*

Between the senses on one side and the “effector” mechanisms on the other, there must be something that bridges the gap, something that uses the information the senses have gained. Even bacteria have this layout, as the case of E. coli showed us. Animals have more complex senses, engage in more complex actions, and possess more complex machinery linking their senses and their actions. According to the sensory-motor view, though, the go-between role has always been central to nervous systems – central at the beginning, central now, and at all stages on the way.

This first view is so intuitive that it might seem there’s no room for an alternative. But there is another picture, easier to lose sight of than the first. Modifying your actions in response to events going on outside you has to be done, yes, but something else has to happen, too, and in some circumstances it is more basic and more difficult to achieve. This is creating actions themselves. How is it that we are able to act in the first place?

Just above, I said: you sense what’s going on and do something in response. But doing something, if you are made of many cells, is not a trivial matter, not something that can simply be assumed. It takes a great deal of coordination between your parts. This is not a big deal if you are a bacterium, but if you’re a larger organism, things are different. Then you face the task of generating a coherent whole-organism action from the many tiny outputs – the tiny contractions, contortions, and twitches – of your parts. A multitude of micro-actions must be shaped into a macro-action.

This is familiar to us in social situations as the problem of teamwork. The players on a football team must combine their actions into a whole, and at least in some kinds of football, this would be a substantial task even if the other team always never varied its moves. An orchestra must solve the same problem. The problem that teams and orchestras face is confronted by some individual organisms, too. This issue is largely peculiar to animals; it’s a problem for multicellular organisms, not single-celled ones, and only a problem for those multicellular organisms whose lifestyle involves complex actions. It’s not much of a problem for bacteria, and not a big problem for seaweed.

Above I treated interactions between neurons as a kind of signaling. Though the analogy is not complete, it is helpful again here as a way of understanding these two visions of the role of early nervous systems. Recall the story of the ride of Paul Revere at the start of the American Revolution in 1775, as told (with considerable poetic license) by Henry Wadsworth Longfellow. The sexton of the Old North Church in Boston was able to observe the movements of the British Army, and he used a lantern code to send a message to Paul Revere (“one if by land; two if by sea”). The sexton was like a sensor, Revere like a muscle, and the sexton’s lantern acted like a nervous connection.

The story of Revere is often used to get people to think about communication in an exact way. And so it does. But it also nudges us toward thinking about a particular kind of communication, which solves a particular kind of problem. Consider a different, though still familiar, situation. Suppose you are in a boat with several rowers, each with one oar. The rowers together can propel the boat forward, but even if they are vigorous, their individual actions will not get the boat to go anywhere unless they coordinate what they’re doing. It doesn’t matter exactly when they pull their oar, as long as they pull at the same time. One way to deal with this situation is to have someone call the “stroke.”

Communication in everyday life serves both roles: there is a sexton-and-Revere or sensory-motor role, based on a division between those who see and those who act, and there is a purely coordinative role, as seen in the rowers. Both of these roles can be played at the same time and there’s no conflict between them. Getting a boat to move requires the coordination of micro-actions, but someone also needs to watch where the boat is going. The person calling the stroke, the coxswain or “cox,” usually acts as the crew’s eyes and as a coordinator of micro-actions. The same combination can be seen in a nervous system.

Though there’s no essential clash between these roles, the distinction itself is important. Through much of the twentieth century, a sensory-motor view of the evolution of nervous systems was simply assumed, and it took some time for the second view, the one based on internal coordination, to become clear. Chris Pantin, an English biologist, developed the second view in the 1950s and it has been revived recently by Fred Keijzer, a philosopher. They rightly point out that it’s easy to fall into the habit of thinking of each “action” as a single unit, in which case the only problem left to solve is coordinating these acts with the senses, working out when to do X rather than Y. As organisms get bigger and can do more, that picture becomes more and more inaccurate. It ignores the problem of how an organism is able to do X or Y in the first place. Pressing an alternative to the sensory-motor theory was a good thing. I’ll call this the action-shaping view of the role played by early nervous systems.

Returning to the history, what did the first animals with nervous systems look like? How should we picture their lives? We don’t yet know. Much of the research in this area has been focused on the cnidarians (pronounced “nye-dair-ians”), a group of animals that includes jellyfish, anemones, and corals. They are very distantly related to us, but not as distantly as sponges, and they do have nervous systems. Though the early branchings in the tree of animals remain murky, it is common to think that the animal with the first nervous system might have been jellyfish-like – something soft, with no shell or skeleton, probably hovering in the water. Picture a filmy lightbulb in which the rhythms of nervous activity first began.

This might have occurred something like 700 million years ago. That date is based entirely on genetic evidence; there are no fossils of animals this old. From looking at rocks of this age, you’d think that all was still and silent. But DNA evidence strongly suggests that many of the crucial branching points in the history of animals must have occurred around that time, and that means that animals were doing something back then. The uncertainty about these crucial stages is frustrating for someone who wants to understand the evolution of brains and minds. As we get a little closer to the present, the picture starts to become clearer.

~ The Garden

In 1946, an Australian geologist, Reginald Sprigg, was exploring some abandoned mines in the outback of South Australia. Sprigg had been sent to find out whether some of the mines might be worth working again. He was several hundred miles from the nearest sea, in a remote area called the Ediacara Hills. Sprigg was eating his lunch, the story has it, when he turned over a rock and noticed what looked like some delicate fossils of jellyfish. As a geologist, he knew the rocks were so old that the finding was important. But he was not an established researcher of fossils, and when he wrote up his paper, few people took it seriously. The journal Nature rejected it, and Sprigg then worked his way down from journal to journal, until his article on what he called “Early Cambrian (?) Jellyfishes” appeared in the Transactions of the Royal Society of South Australia in 1947, alongside such papers as “On the Weights of Some Australian Mammals.” The paper had a quiet career at first, and it took another decade or so before anyone realized what Sprigg had found.

At the time, scientists familiar with the fossil record were well aware of the importance of the Cambrian period, which began about 542 million years ago. In the “Cambrian explosion,” a great range of the animal body plans we know today first appeared. Sprigg’s discoveries turned out to be the first fossil record of animals living before that time. Sprigg did not realize this in 1947 – he dated his jellyfish as early Cambrian. But as similar fossils were found in other places around the world and people took more note of Sprigg’s outback jellyfish, it became clear that they dated from well before the Cambrian, and were probably not jellyfish, in most cases, at all. The period in prehistory now known as the Ediacaran (named after the hills Sprigg was exploring, and pronounced “Eedee-ac-aran”) runs from 635 to about 542 million years ago. With the Ediacaran fossils we get our first direct evidence of what the lives of very early animals might have been like – how big they were, how numerous, how they lived.

The nearest large city to Sprigg’s site is Adelaide, where a large collection of Ediacaran fossils is kept in the South Australian Museum. I was shown around the exhibits by Jim Gehling, who knew Sprigg and has worked on the fossils since 1972. I was surprised at how dense with life the ancient environment was; the Ediacaran was not about a few lone individuals. Many rock slabs Gehling has collected contain dozens of fossils of different sizes. Among the more prominent is Dickinsonia, which has fine stripe-like segments and looks a bit like a lily pad, or a bath mat. (A picture of a Dickinsonia in the South Australian Museum’s collection appears just below this paragraph.) But if you focus on the large fossils, you miss most of the life that is present. Several times, Gehling walked up to what looked like a scrappy and nondescript bit of one of the rocks and pressed a piece of Silly Putty into it; when he took it back, the putty revealed a fine and detailed imprint of a tiny animal.


Ediacaran animals weren’t tiny – many were several inches in length, some up to three feet. They seem to have mostly lived on the sea floor, on and amid mats made of living material – clods of bacteria and other microbes. Their world was a kind of undersea swamp. Many were probably motionless as adults, anchored in place. Some might have been early sponges and corals. Others had body forms that have since been entirely abandoned by evolution – three-sided and four-sided designs, some with quilted arrangements of plant-like fronds. Many Ediacarans seem to have lived quiet lives of very limited mobility on the bottom of the sea.

DNA evidence, though, suggests strongly that there were nervous systems present at this time – probably in some of the animals on the wall in Adelaide. Which ones? Among them are some animals who appear to have moved under their own steam. The clearest case is Kimberella. This animal, which I have drawn below, seems to have looked like the top half of a macaron, though a macaron that was oval, with a front and back, and perhaps with a tongue-like appendage on one end. The traces it left suggest that it pushed the sediment before it as it moved, and scratched the surfaces it crawled over, perhaps in feeding. Kimberella is sometimes interpreted as a mollusk, or perhaps a member of an abandoned evolutionary line close to the mollusks. If Kimberella could crawl, then, especially as it grew to several inches long, it almost certainly had a nervous system.


Kimberella seems the clearest case of a self-propelled Ediacaran, but there were very likely others. Near a Dickinsonia fossil, one often finds a sequence of fainter traces bearing the same shape. The animal seemed to sit and feed for a while at one spot, then move on. Some reconstructions of Ediacaran scenes show a few animals swimming, including Spriggina, named after Reg, their discoverer, but Gehling thinks this scenario is unlikely, because Spriggina fossils are always found the same way up. If a Spriggina swam, then whenever some tiny disaster killed it, it would have had some chance of landing the other way up. So Gehling thinks that Spriggina, like Kimberella, crawled.

Some biologists have argued that the Ediacarans are members of an animal-like evolutionary experiment, but not properly animals themselves. Rather than sitting on the animal branch of the tree of life, they exhibit a different way that cells can come together to yield an organism. Those strange three-sided forms and quilted fronds might support such a view. A more standard interpretation is that some Ediacarans, like Kimberella, were members of familiar animal groups, while other fossils represent abandoned evolutionary detours, together with ancient algae and other kinds of life. One theme that has emerged fairly consistently, though, is that the Ediacaran world was a rather peaceful one, a world largely without conflict and predation.

The word “peace” might not be apt, as it suggests a kind of considered friendship or truce. Rather, the Ediacarans appear to have had very little to do with each other. They munched on the mat, filtered food from the water, and in some cases roamed around, but if the fossil evidence is any guide, they hardly interacted at all.

Perhaps the fossil record is not a good guide; back in the first part of this chapter I discussed how the world of single-celled organisms now seems full of hidden interactions, mediated by chemical signals. The same may have been true in Ediacaran times, and this mode of interaction would leave no fossil trace. And certainly the Ediacarans competed with each other in an evolutionary sense – that is inevitable in a world of reproducing organisms. But some of the most conspicuous forms of interaction between one organism and another do seem to be absent. In particular, there is no evidence of predation – no half-eaten animal remains. (A few fossils show possible signs of predation-related damage in one animal, Cloudina, but even this case is unclear.) This was in no sense a dog-eat-dog world. Instead, in a phrase coined by the American paleontologist Mark McMenamin, it seems to have been “the Garden of Ediacara.”

We can also learn something about life in the garden from Ediacaran bodies. These creatures do not seem to have large and complex sense organs. There are no large eyes, no antennae. Almost certainly they had some responsiveness to light and chemical traces, but they made little investment, as far as we can tell, in this sort of machinery. There are also no claws, spikes or shells – no weapons, and no shields with which to fend weapons off. Their lives seem not to have been lives of conflict and complicated interaction; they certainly didn’t evolve the familiar tools used in such interactions. It was a garden of relatively self-contained and self-possessed beings. Macarons that pass in the night.

This is vastly unlike animal life now. Our animal cousins are highly alert to their environment; they track friends, foes, and countless other features of the landscape. They do that because what’s going on around them matters; often it’s a matter of life and death. Ediacaran lives show no evident sign of this moment-to-moment engagement with the environment. If so, this makes it likely that our Ediacaran ancestors put their nervous systems – when they had them – to different uses from those seen in more recent animals. Specifically, this might have been a time when the role played by those nervous systems fits the second of the theories of nervous system evolution I introduced above, the view based on internal coordination rather than sensory-motor control. Nervous systems were for shaping movements, maintaining rhythms, crawling and (perhaps) swimming. This would have included some sensing of the environment, but perhaps not very much.

Those inferences might be mistaken; perhaps a great deal of sensing and interaction was going on, using organs made of soft materials that leave no trace. Something else that has always puzzled me in discussions of the peaceful Ediacaran is the role of jellyfish. Sprigg’s own fossils were not jellyfish, as he’d thought, but jellyfish are believed to have been around at this time, usually leaving no traces. Cnidarians in general, but especially jellyfish, have stinging cells, and a garden of stinging jellyfish, as any Australian will insist, is far from Edenic.

When the Royal Society of London held a conference on early animals and the first nervous systems in 2015, the age of the first jellyfish stings was a topic of puzzled discussion. It does seem that cnidarian stings evolved early – this we infer from the fact that the evolutionary split between two major branches of this group appears to date to the Ediacaran or even before, and animals on both sides of the split have the same sort of stingers. Cnidarian stings are weapons. Were they offensive or defensive? Neither the prey nor the foes of modern cnidarians existed back then. So who were the stings aimed at? We do not know.

Even if Ediacaran life was not as peaceful as has sometimes been supposed, a very different world was around the corner.

The “Cambrian explosion” began around 542 million years ago. In a relatively sudden series of events, most of the basic animal forms seen today arose. These “basic animal forms” did not include mammals, but did include vertebrates, in the form of fish. They also included arthropods – animals with an external skeleton and limbs with joints, such as trilobites – along with worms, and various others.

Why did it happen then, and why did it happen so fast? The timing may have had to do with changes to the Earth’s chemistry and climate. But the process itself may have been largely driven by a kind of evolutionary feedback, due to interactions between organisms themselves. In the Cambrian, animals became part of each other’s lives in a new way, especially through predation. This means that when one kind of organism evolves a little, it changes the environment faced by other organisms, which evolve in response. From the early Cambrian onward there was definitely predation, together with everything that predation encourages: tracking, chasing, defending. When prey starts to hide or defend itself, predators improve their ability to track and subdue, leading in turn to better defenses on the prey side. An “arms race” has begun. From the early part of the Cambrian, the fossil record of animal bodies contains exactly what was not seen in the Ediacaran – eyes, antennae, and claws. The evolution of nervous systems was heading down a new path.

The revolution in behavior seen in the Cambrian also occurred, in large part, through the unfolding of possibilities inherent in a particular kind of body. A jellyfish has a top and bottom but no left and right. It is said to have radial symmetry. But humans, fish, octopuses, ants, and earthworms are all bilaterians, or bilaterally symmetrical animals. We have a front and back, and hence a left and right, as well as a top and bottom. The first bilaterians, or at least some early ones, might have looked bit like this:


I have given the animal eyespots on each side of its “head,” though this is controversial (and those eyes are exaggerated in the picture – they would probably have been tiny). I am being generous to the early bilaterians.

Several Ediacaran animals are believed to be bilaterians, including Kimberella, pictured a few pages back. If Kimberella was a bilaterian, then bilaterians before the Cambrian were already living somewhat more active lives than other animals. But in the Cambrian, they were unstoppable. The bilaterian body plan makes for mobility (walking is a very bilateral thing to do), and this body plan is friendly, it turns out, to many kinds of complex behavior. The diversification and entanglement of lives that took place in the Cambrian was mostly the work of bilaterians.

Before pressing on into the world of bilaterian evolution, let’s pause and ask: which animal produces the most sophisticated behavior, which is the smartest, without a bilaterian body plan? Questions like this are notoriously hard to answer in an unbiased way, but in this case, the answer is clear. The most behaviorally sophisticated animals outside the bilaterians are the – terrifying – box jellyfish, the Cubozoa.

With their soft bodies and sparse fossil record, it is hard to work out when different kinds of jellyfish evolved, but cubozoans are thought to be late arrivals, originating in the Cambrian or after. A general feature of cnidarians, as I noted above, is their stinging cells. Some cubozoans have truly brutal venom in their stingers, strong enough to have killed large numbers of humans. In northeastern Australia, the presence of box jellyfish clears the beaches completely each summer; for a good part of the year it’s too dangerous to swim off the shore at all, except in netted enclosures. To compound the problem, these jellyfish are invisible in the water. They also have the most complex behaviors of any non-bilaterian. Around the top of their body are two dozen sophisticated eyes – eyes with lenses and retinas, like ours. The Cubozoa can swim at about three knots, and some can navigate by watching external landmarks on the shore. Box jellyfish, the lethal behavioral pinnacle of non-bilaterian evolution, are also products of the new world that began in the Cambrian.

~ Senses

Nervous systems evolved before the bilaterian body plan, but this body created vast new possibilities for their use. During the Cambrian the relations between one animal and another became a more important factor in the lives of each. Behavior became directed on other animals – watching, seizing, and evading. From early in the Cambrian we see fossils that display the machinery of these interactions: eyes, claws, antennae. These animals also have obvious marks of mobility: legs and fins. Legs and fins don’t necessarily show that one animal was interacting with others. Claws, in contrast, have little ambiguity.

In the Ediacaran, other animals might be there around you, without being especially relevant. In the Cambrian, each animal becomes an important part of the environment of others. This entanglement of one life in another, and its evolutionary consequences, is due to behavior and the mechanisms controlling it. From this point on, the mind evolved in response to other minds.

When I say that, you might reply that the term “mind” is out of place. In this chapter, I won’t argue with that. Fine. What is the case, though, is that the senses, the nervous systems, and the behaviors of each animal began to evolve in response to the senses, nervous systems, and behaviors of others. The actions of one animal created opportunities for and demands on others. If a yard-long, fast-swimming anomalocarid is swooping down toward you, like a giant predatory cockroach with two grasping appendages on its head poised and ready, it’s a very good thing to know, somehow, that this is happening, and to take evasive action.

The senses may well have been crucial to the Cambrian: organisms opened up to the world, especially to each other. The first sophisticated eyes seem to have appeared, eyes that can form an image. The Cambrian witnessed the appearance of both the compound eyes seen today in insects and camera eyes like our own. Imagine the behavioral and evolutionary consequences of being able to see the objects around you for the first time, especially objects at some distance and in motion. The biologist Andrew Parker has argued that the invention of eyes was the decisive event in the Cambrian. Others have developed broader views, but with a similar flavor. As the paleontologist Roy Plotnick and his colleagues put it, the result of this sensory opening was a “Cambrian information revolution.” With an influx of sensory information comes a need for complex internal processing. When more is known, decisions become more complicated. (Is the anomalocarid more likely to intercept me if I flee to that hole, or that other one?) An image-forming eye makes possible actions that would be unthinkable without it.

Jim Gehling, my Ediacaran guide, and the British paleontologist Graham Budd have offered scenarios for how the feedback process generating these changes got under way. Near the close of the Ediacaran, Gehling suspects that scavenging arose, followed by predation. Animals went from feeding on microbial mats to feeding on the dead, and then began hunting the living. As Budd sees it, animal behavior itself changed the way resources were distributed in the Ediacaran. Imagine a world with edible microbial mats stretching before you like an endless swampy lawn. Slow-moving grazers wander over the mats, consuming this rather uniform resource. Other animals fed without moving. These animals then become a new kind of resource; they are big concentrations of nutritious carbon compounds. Nutrition is now less spread out than it was. It exists in patches. These animals might first have only been consumed by others after they had died. But this soon changed. Scavenging became predation.

If the fossil record is taken at face value, it seems that one group set the pace: the arthropods. This group today includes insects, crabs, and spiders. Early in the Cambrian we see the rise of trilobites, which are prototypical arthropods with shells, jointed legs, and compound eyes. In the photograph of the Dickinsonia fossil on page 29, you’ll find two much smaller fossils just below it, above the letters “A” and “B.” These animals are just millimeters long, and Gehling thinks they might be precursors of trilobites – still soft-bodied, but with hints of a trilobite design. In this picture, Dickinsonia is present in its classic Ediacaran mode, with no apparent limbs, head, or protection, while purposeful little bugs lurk beneath. The image reminds me of a drawing in a book about the dinosaurs and their decline that I owned as a child. A huge dinosaur towered over a few small and mischievous-looking mammals, shrew-like creatures, at its feet. I think they had their eye on a clutch of dinosaur eggs. The trilobite precursors look intent on a similar goal, with the lilypad-bathmat Dickinsonia oblivious above.

Michael Trestman, another philosopher, has offered an interesting way of looking at all these animals. Consider, he says, the category of animals who have complex active bodies. These are animals who can move quickly, and who can seize and manipulate objects. Their bodies have appendages that can move in many directions, and they have senses, such as eyes, which can track distant objects. Trestman says that only three of the major animal groups produced some species with complex active bodies (CABs). Those groups are arthropods, chordates (animals like us with a nerve cord down their back), and one group of mollusks, the cephalopods. This trio might seem to make up a large category, because these are the sorts of animals that tend to come to our minds, but it is a small group in many ways. There are about thirty-four animal phyla – basic animal body plans. Only three phyla contain some animals with CABs, and within one of those three, the mollusks, the only animals that count are cephalopods.

With these ancient stages of the historical story in place, I’ll return to the divide between two views of nervous systems and their evolution – the sensory-motor and action-shaping views. Earlier I introduced the distinction, linked it to two roles that signals can have in social life (sexton and Revere versus the rowboat), and noted that the two roles are different but also compatible. What might be the historical significance of this divide? Can the distinction be fit in some natural way onto the march of millennia from the Ediacaran, to the Cambrian, to more recent times? It does seem possible that there was a shift in the roles nervous systems were performing. Although tracking events in the outside world might always be worth doing to some extent, the Cambrian sees a great increase in the importance of this side of life. There’s more that’s worth watching, and more that needs to be done in response to what’s seen. Not paying attention, for the first time, means getting eaten by the swooping anomalocarid. Perhaps, then, the very first nervous systems primarily served to coordinate actions – first animating the body of an ancient cnidarian, then shaping the actions of Ediacarans. But if there was such an era, by the Cambrian it was over.

This is one possibility among many, though, and our imaginations, shaped by lives lived in modern bodies, underestimate the range of options. Possibilities abound. Here is one developed by the biologist Detlev Arendt and his colleagues. As they see it, nervous systems originated twice. But they don’t mean that they evolved in two kinds of animals; rather, they originated twice in the same animals, at different places in the animal’s body. Imagine a jellyfish-like animal shaped like a dome, with a mouth underneath. One nervous system evolves on the top, and tracks light, but not as a guide to action. Instead it uses light to control bodily rhythms and regulate hormones. Another nervous system evolves to control movement, initially just the movement of the mouth. And at some stage, the two systems begin to move within the body, coming into new relations with each other. Arendt sees this as one of the crucial events that took bilaterians forward in the Cambrian. A part of the body-controlling system moved up toward the top of the animal, where the light-sensitive system sat. This light-sensitive system, again, was only guiding chemical changes and cycles, not behavior. But the joining of the two nervous systems gave them a new role.

What an amazing image: in a long evolutionary process, a motion-controlling brain marches up through your head to meet there some light-sensitive organs, which become eyes.

~ The Fork

The bilaterian body plan arose before the Cambrian, in some small and unremarkable form, but it became the bodily scaffold on which a long series of increases in behavioral complexity was laid down. Early bilaterians also have another role in this book. Sometime soon after they appeared, probably still in the Ediacaran, there was a branching, one of the countless evolutionary forks that take place as the millennia pass. A population of these animals split into two. The animals who initially wandered off down the two paths might have looked like small flattened worms. They had neurons, and perhaps very simple eyes, but little of the complexity that was to come. Their scale was measured perhaps in millimeters.

After this innocuous split, the animals on each side diverged, and each became ancestor to a huge and persisting branch of the tree of life. One side led to a group that includes vertebrates, along with some surprising companions such as starfish, while the second side led to a huge range of other invertebrate animals. The point just before this split is the last point at which an evolutionary history is shared between ourselves and the big group of invertebrates that includes beetles, lobsters, slugs, ants, and moths.

Here is a diagram of this part of the tree of life. Lots of groups are omitted from the picture, both outside and inside the branches shown. The moment we’re talking about is labeled “the fork.”


On each path downstream of the fork, more branchings occurred. One side eventually sees fish appear, then dinosaurs and mammals. This is our side. On the other side, further branchings give rise to arthropods, mollusks, and others. On both sides, passing from the Ediacaran into the Cambrian and beyond, lives become entangled, the senses open, and nervous systems expand. Until, in one tiny example of this sensory and behavioral entangling, a rubber-encased mammal and a color-changing cephalopod find themselves staring at each other in the Pacific Ocean.

* If you’ve seen the word “sensorimotor” instead, please treat this as the same.

Other Minds: The Octopus and the Evolution of Intelligent Life

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