Other Minds: The Octopus and the Evolution of Intelligent Life

Two Meetings and a Departure

On a spring morning in 2009, Matthew Lawrence dropped the anchor of his small boat at a random spot in the middle of a blue ocean bay on the east coast of Australia, and jumped over the side. He swam down on scuba to where the anchor lay, picked it up, and waited. The breeze on the surface nudged the boat, which started to drift, and Matt, holding the anchor, followed.

This bay is well-known for diving, but divers usually visit only a couple of spectacular locations. As the bay is large and typically pretty calm, Matt, a scuba enthusiast who lives nearby, had begun a program of underwater exploration, letting the breeze carry the empty boat around above him until his air ran out and he swam back up the anchor line. On one of these dives, roaming over a flat sandy area scattered with scallops, he came across something unusual. A pile of empty scallop shells – thousands of them – was roughly centered around what looked like a single rock. On the shell bed were about a dozen octopuses, each in a shallow, excavated den. Matt came down and hovered beside them. The octopuses each had a body about the size of a football, or smaller. They sat with their arms tucked away. They were mostly brown-gray, but their colors changed moment by moment. Their eyes were large, and not too dissimilar to human eyes, except for the dark horizontal pupils – like cats’ eyes turned on their side.

The octopuses watched Matt, and also watched one another. Some started roaming around. They’d haul themselves out of their dens and move over the shell bed in an ambling shuffle. Sometimes this elicited no response from others, but occasionally a pair would dissolve into a multi-armed wrestle. The octopuses seemed to be neither friends nor enemies, but in a state of complicated coexistence. As if the scene were not sufficiently strange, many baby sharks, each just six inches or so long, lay quietly on the shells as the octopuses roamed around them.

A couple of years before this I was snorkeling in another bay, in Sydney. This site is full of boulders and reefs. I saw something moving under a ledge – something surprisingly large – and went down to look at it. What I found looked like an octopus attached to a turtle. It had a flat body, a prominent head, and eight arms coming straight from the head. The arms were flexible, with suckers – roughly like octopus arms. Its back was fringed with something that looked like a skirt, a few inches wide and moving gently. The animal seemed to be every color at once – red, gray, blue-green. Patterns came and went in a fraction of a second. Amid the patches of color were veins of silver like glowing power lines. The animal hovered a few inches above the sea floor, and then came forward to look at me. As I had suspected from the surface, this creature was big – about three feet long. The arms roved and wandered, the colors came and went, and the animal moved forward and back.

This animal was a giant cuttlefish. Cuttlefish are relatives of octopuses, but more closely related to squid. Those three – octopuses, cuttlefish, squid – are all members of a group called the cephalopods. The other well-known cephalopods are nautiluses, deep-sea Pacific shellfish which live quite differently from octopuses and their cousins. Octopuses, cuttlefish, and squid have something else in common: their large and complex nervous systems.

I swam down repeatedly, holding my breath, to watch this animal. Soon I was exhausted, but I was also reluctant to stop, as the creature seemed as interested in me as I was in it (in him? in her?). This was my first experience with an aspect of these animals that has never stopped intriguing me: the sense of mutual engagement that one can have with them. They watch you closely, usually maintaining some distance, but often not very much. Occasionally, when I’ve been very close, a giant cuttlefish has reached an arm out, just a few inches, so it touches mine. It’s usually one touch, then no more. Octopuses show a stronger tactile interest. If you sit in front of their den and reach out a hand, they’ll often send out an arm or two, first to explore you, and then – absurdly – to try to haul you into their lair. Often, no doubt, this is an overambitious attempt to turn you into lunch. But it’s been shown that octopuses are also interested in objects that they pretty clearly know they can’t eat.

To understand these meetings between people and cephalopods, we have to go back to an event of the opposite kind: a departure, a moving apart. The departure happened quite some time before the meetings – about 600 million years before. Like the meetings, it involved animals in the ocean. No one knows what the animals in question looked like in any detail, but they perhaps had the form of small, flattened worms. They may have been just millimeters long, perhaps a little larger. They might have swum, might have crawled on the sea floor, or both. They might have had simple eyes, or at least light-sensitive patches, on each side. If so, little else may have defined “head” and “tail.” They did have nervous systems. These might have comprised nets of nerves spread throughout the body, or they might have included some clustering into a tiny brain. What these animals ate, how they lived and reproduced – all are unknown. But they had one feature of great interest from an evolutionary point of view, a feature visible only in retrospect. These creatures were the last common ancestors of yourself and an octopus, of mammals and cephalopods. They’re the “last” common ancestors in the sense of most recent, the last in a line.

The history of animals has the shape of a tree. A single “root” gives rise to a series of branchings as we follow the process forward in time. One species splits into two, and each of those species splits again (if it does not die out first). If a species splits, and both sides survive and split repeatedly, the result may be the evolution of two or more clusters of species, each cluster distinct enough from the others to be picked out with a familiar name – the mammals, the birds. The big differences between animals alive now – between beetles and elephants, for example – originated in tiny insignificant splits of this sort, many millions of years ago. A branching took place and left two new groups of organisms, one on each side, that were initially similar to each other, but evolved independently from that point on.

You should imagine a tree that has an inverted triangular, or conical, shape from far away, and is very irregular inside – something like this:

Now imagine sitting on a branch on top of the tree, looking down. You are on the top because you’re alive now (not because you are superior), and around you are all the other organisms alive now. Close to you are your living cousins, such as chimpanzees and cats. Further away, as you look horizontally across the top of the tree, you’ll see animals that are more distantly related. The total “tree of life” also includes plants and bacteria and protozoa, among others, but let’s confine ourselves to the animals. If you now look down the tree, toward the roots, you’ll see your ancestors, both recent ones and those more remote. For any pair of animals alive now (you and a bird, you and a fish, a bird and a fish), we can trace two lines of descent down the tree until they meet in a common ancestor, an ancestor of both. This common ancestor might be encountered just a short way down the tree, or further down. In the case of humans and chimps we reach a common ancestor very quickly, living about six million years ago. For very different pairs of animals – human and beetle – we have to trace the lines further down.

As you sit in the tree, looking across at your near and distant relatives, consider a particular collection of animals, the ones we usually think of as “smart” – the ones with large brains, who are complex and flexible in their behavior. These will certainly include chimps and dolphins, also dogs and cats, along with humans. All these animals are quite near to you on the tree. They are fairly close cousins, from an evolutionary point of view. If we’re doing this exercise properly we should also add birds. One of the most important developments in animal psychology over the last few decades has been the realization of how smart crows and parrots are. Those are not mammals, but they are vertebrates, and hence they are still fairly close to us, though not nearly as close as chimps. Having collected all these birds and mammals, we can ask: What was their most recent common ancestor like, and when did it live? If we look down the tree to where their lines of ancestry all fuse, what do we find living there?

The answer is a lizard-like animal. It lived something like 320 million years ago, a bit before the age of the dinosaurs. This animal had a backbone, was of reasonable size, and was adapted to life on land. It had an architecture similar to our own, with four limbs, a head, and a skeleton. It walked around, used senses similar to ours, and had a well-developed central nervous system.

Now let’s look for the common ancestor that connects this first group of animals, which includes ourselves, to an octopus. To find this animal we have to travel much further down the branches. When we find it, about 600 million years before the present, the animal is that flattened worm-like creature I sketched earlier.

This step back in time is nearly twice as long as the step we took to find the common ancestor of mammals and birds. The human-octopus ancestor lived at a time when no organisms had made it onto land and the largest animals around it might have been sponges and jellyfish (along with some oddities I’ll discuss in the next chapter).

Assume we’ve found this animal, and are now watching the departure, the branching, as it happened. In a murky ocean (on the sea floor, or up in the water column) we’re watching a lot of these worms live, die, and reproduce. For an unknown reason, some split off from the others, and through an accumulation of happenstance changes they start to live differently. In time, their descendants evolve different bodies. The two sides split again and again, and before long we are looking not at two collections of worms, but at two enormous branches of the evolutionary tree.

One path forward from that underwater split leads to our branch of the tree. It leads to vertebrates, among others, and within the vertebrates, to mammals and eventually humans. The other path leads to a great range of invertebrate species, including crabs and bees and their relatives, many kinds of worms, and also the mollusks, the group that includes clams, oysters, and snails. This branch does not contain all the animals commonly known as “invertebrates,” but it does include most of the familiar ones: spiders, centipedes, scallops, moths.

In this branch most of the animals are fairly small, with exceptions, and they also have small nervous systems. Some insects and spiders engage in very complex behavior, especially social behavior, but they still have small nervous systems. That’s how things go in this branch – except for the cephalopods. These are a subgroup within the mollusks, so they are related to clams and snails, but they evolved large nervous systems, and the ability to behave in ways very different from other invertebrates. They did this on an entirely separate evolutionary path from ours.

Cephalopods are an island of mental complexity in the sea of invertebrate animals. Because our most recent common ancestor was so simple and lies so far back, cephalopods are an independent experiment in the evolution of large brains and complex behavior. If we can make contact with cephalopods as sentient beings, it is not because of a shared history, not because of kinship, but because evolution built minds twice over. This is probably the closest we will come to meeting an intelligent alien.

~ Outlines

One of the classic problems of my discipline – philosophy – is the relation between mind and matter. How do sentience, intelligence, and consciousness fit into the physical world? I want to make progress on that problem, vast as it is, in this book. I approach the problem by following an evolutionary road; I want to know how consciousness arose from the raw materials found in living beings. Aeons ago, animals were just one of various unruly clumps of cells that started living together as units in the sea. From there, though, some of them took on a particular lifestyle. They went down a road of mobility and activity, sprouting eyes, antennae, and means to manipulate objects around them. They evolved the creeping of worms, the buzzing of gnats, the global voyages of whales. As part of all this, at some unknown stage, came the evolution of subjective experience. For some animals, there’s something it feels like to be such an animal. There is a self, of some kind, that experiences what goes on.

I am interested in how experience of all kinds evolved, but cephalopods will have special importance in this book. This is firstly because they are such remarkable creatures. If they could talk, they could tell us so much. That is not the only reason they clamber and swim through the book, though. These animals shaped my path through the philosophical problems; following them through the sea, trying to work out what they’re doing, became an important part of my route in. In approaching questions about animal minds, it is easy to be influenced too much by our own case. When we imagine the lives and experiences of simpler animals, we often wind up visualizing scaled-down versions of ourselves. Cephalopods bring us into contact with something very different. How does the world look to them? An octopus’s eye is similar to ours. It is formed like a camera, with an adjustable lens that focuses an image on a retina. The eyes are similar but the brains behind them are different on almost every scale. If we want to understand other minds, the minds of cephalopods are the most other of all.

Philosophy is among the least corporeal of callings. It is, or can be, a purely mental sort of life. It has no equipment that needs managing, no sites or field stations. There’s nothing wrong with that – the same is true of mathematics and poetry. But the bodily side of this project has been an important side. I came across the cephalopods by chance, by spending time in the water. I began following them around, and eventually started thinking about their lives. This project has been much affected by their physical presence and unpredictability. It has also been affected by the myriad practicalities of being underwater – the demands of gear and gases and water pressure, the easing of gravity in the green-blue light. The efforts a human must make to cope with these things reflect differences between life on land and in water, and the sea is the original home of the mind, or at least of its first faint forms.

At the start of this book I placed an epigraph from the philosopher and psychologist William James, writing at the end of the nineteenth century. James wanted to understand how consciousness came to inhabit the universe. He had an evolutionary orientation to the issue, in a broad sense that included not just biological evolution but the evolution of the cosmos as a whole. He thought that we need a theory based on continuities and comprehensible transitions; no sudden entrances or jumps.

Like James, I want to understand the relation between mind and matter, and I assume that a story of gradual development is the story that has to be told. At this point, some might say that we already know the outlines of the story: brains evolve, more neurons are added, some animals become smarter than others, and that’s it. To say that, though, is to refuse to engage with some of the most puzzling questions. What are the earliest and simplest animals that had subjective experience of some kind? Which animals were the first to feel damage, feel it as pain, for example? Does it feel like something to be one of the large-brained cephalopods, or are they just biochemical machines for which all is dark inside? There are two sides to the world that have to fit together somehow, but do not seem to fit together in a way that we presently understand. One is the existence of sensations and other mental processes that are felt by an agent; the other is the world of biology, chemistry, and physics.

Those problems won’t be entirely resolved in this book, but it’s possible to make progress on them by charting the evolution of the senses, bodies, and behavior. Somewhere in that process lies the evolution of the mind. So this is a philosophy book, as well as a book about animals and evolution. That it’s a philosophy book does not place it in some arcane and inaccessible realm. Doing philosophy is largely a matter of trying to put things together, trying to get the pieces of very large puzzles to make some sense. Good philosophy is opportunistic; it uses whatever information and whatever tools look useful. I hope that as the book goes along, it will move in and out of philosophy through seams that you won’t much notice.

The book aims, then, to treat the mind and its evolution, and to do so with some breadth and depth. The breadth involves thinking about different sorts of animals. The depth is depth in time, as the book embraces the long spans and successive regimes in the history of life.

The anthropologist Roland Dixon attributed to the Hawaiians the evolutionary tale I used as my second epigraph: “At first the lowly zoophytes and corals come into being, and these are followed by worms and shellfish, each type being declared to conquer and destroy its predecessor …” The story of successive conquests that Dixon outlines is not how the history really went, and the octopus is not the “lone survivor of an earlier world.” But the octopus does have a special relation to the history of the mind. It is not a survivor but a second expression of what was present before. The octopus is not Ishmael from Moby-Dick, who escaped alone to tell the tale, but a distant relative who came down another line, and who has, consequently, a different tale to tell.

2

A HISTORY OF ANIMALS (#uc649e0bc-c791-58d5-b7fb-d93d8bf30ffa)

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.