Introduction
You often wonder what goes on inside the minds of other creatures, especially when you look into the eye of an octopus. You face a wall of silence because their evolutionary path diverged from yours half a billion years ago.
Cephalopods evolved large brains and sophisticated sentience along an evolutionary path completely independent from vertebrates, offering a rare glimpse into an alternate intelligence.
Peter Godfrey-Smith traces this journey from the origin of multicellular life and the earliest nervous systems to the soft-bodied innovations of squids and octopuses. You will explore how distributed nervous systems, color-changing skin, and complex social interactions create a wholly different kind of sentience.
- How did subjective experience first emerge in the oceans?
- What does it feel like to think with your arms?
- Why do animals with such immense intelligence live such short lives?
1. Meetings Across the Tree of Life
Peter Godfrey-Smith describes an underwater encounter with a three-foot-long giant cuttlefish in Sydney. The animal hovered above the sea floor, displayed rapid color changes and veins of silver, and approached him with roving arms.
The last common ancestor of humans and octopuses lived approximately 600 million years ago and was likely a small, flattened worm-like creature.
Evolutionary Background
Tracing the evolutionary tree of life backwards reveals that the most recent common ancestor shared by mammals and cephalopods existed roughly 600 million years ago in the ocean. This creature possessed simple light-sensitive patches and a basic nervous system before the lineage split.
By contrast, the most recent common ancestor connecting mammals and birds was a lizard-like vertebrate that lived about 320 million years ago. Humans and chimps shared a common ancestor about six million years ago.
The Second Expression of Mind
Cephalopods represent an independent experiment in the evolution of large brains and complex behavior. They serve as the closest equivalent to meeting an intelligent alien.
An octopus possesses a camera-like eye similar to a vertebrate's, but its brain structure is fundamentally different on almost every scale. You can view the octopus not as a survivor of an earlier primitive world, but as a second independent expression of mental complexity.
Matthew Lawrence dropped an anchor on a random sandy area scattered with scallops and found a dense settlement of octopuses living in shallow excavated dens alongside baby sharks.
2. History of Animals and Nervous Systems
Nervous systems likely evolved for internal physical coordination rather than mere sensory-motor links, sparking a Cambrian arms race.
From Single Cells to Complex Bodies
Single-celled bacteria solve spatial orientation problems by using time to measure changes in chemical concentrations. E. coli bacteria move toward welcome chemicals and away from unwelcome ones by switching between running and tumbling motions, reducing tumbling when detecting increasing food concentrations.
Single-celled organisms use chemical signaling to assess population density and coordinate group behavior. Bacteria living inside Hawaiian squid produce light through a chemical reaction by detecting an inducer molecule to assess population density, helping the host squid with nocturnal camouflage.
While the traditional sensory-motor view posits that nervous systems exist to connect senses with motor output, the action-shaping view argues that complex multicellular organisms needed a mechanism to coordinate countless micro-actions into a coherent macro-action. Biologist Chris Pantin and philosopher Fred Keijzer developed the action-shaping view, comparing early nervous system coordination to the problem faced by a rowing crew or an orchestra.
Nervous systems are extraordinarily expensive biological machines that consume massive amounts of energy. In human beings, nearly a quarter of the energy taken in as food is spent solely on keeping the brain running.
The Cambrian Explosion
The Ediacaran period represented a peaceful undersea epoch largely devoid of active predation and complex sensory interaction. Geologist Reginald Sprigg discovered delicate fossil imprints in the Ediacaran Hills of South Australia in 1946, revealing a dense community of soft-bodied creatures like Dickinsonia and Kimberella, which lasted from 635 to 542 million years ago and reached sizes from several inches to three feet.
The Cambrian explosion triggered an evolutionary arms race driven by predation, sensory evolution, and ecological feedback starting 542 million years ago. Unlike the peaceful Ediacaran fossils, Cambrian fossil records suddenly feature complex body parts explicitly designed for interaction and conflict, such as trilobite shells, compound eyes, claws, and antennae.
Box jellyfish represent the pinnacle of behavioral complexity among non-bilaterian animals. Cubozoans possess two dozen sophisticated eyes with lenses and retinas around their bodies and can swim at speeds of about three knots.
Only a tiny minority of animal phyla produced species with complex active bodies capable of sophisticated manipulation and movement. Philosopher Michael Trestman notes that among approximately thirty-four animal phyla, complex active bodies appear exclusively in arthropods, chordates, and cephalopods.
3. Evolution and Anatomy of Cephalopods
Cephalopods evolved from small, limpet-like shelled mollusks into swimming predators. Early mollusks developed hard cap-shaped shells to escape newly invented predation in the Cambrian period. Later, some of these animals entered the water column, using gas-filled shells as buoyancy devices akin to zeppelins and inventing jet propulsion via a tube-like siphon.
Before the age of dinosaurs, lineages began giving up their external shells. This transition led to internal remnants in cuttlefish and squids, and the complete loss of a shell in octopuses. The nautilus represents the single surviving exception that kept its coiled external shell. Ancient giant predatory cephalopods like Cameroceras reached lengths of eighteen feet before being outcompeted by fish.
By abandoning their external shells, cephalopods gained immense bodily freedom while distributing most of their neurons directly into their arms.
Body of Pure Possibility
Standard theories of embodied cognition argue that an animal's fixed body shape and joint angles naturally constrain and encode information to simplify movement. In contrast, you see that the octopus has a protean body capable of transforming from a towering shape to a liquid-like squeeze through tiny holes. This form operates entirely outside the standard brain-body divide. Researchers like Benny Hochner note that octopuses possess a completely different embodiment compared to vertebrates, characterized by distributed nervous activity across a formless body.
David Scheel taught giant Pacific octopuses to recognize new food sources like clams by partly smashing them. The octopuses then figured out how to pull intact clam shells apart using raw strength. Unlike social insects that achieve complex behaviors through colony coordination, octopuses pursue a non-social, idiosyncratic form of intelligence. Their need to hunt active prey like crabs and extract meat from protective shells or novel obstacles drives their exploratory nature. The sheer neural complexity required to control their jointless, shell-less bodies may have also provided a mental surplus that fuels their problem-solving and playful manipulation of objects.
Distributed Nervous Systems
Unlike vertebrates with centralized brains, the octopus nervous system is largely distributed throughout its body. A common octopus has about 500 million neurons. Roughly twice as many neurons reside in its arms as in its central brain, and the esophagus passes directly through the middle of the central brain.
Each sucker is packed with thousands of neurons handling touch and chemical sensors like taste. This layout allows the arms to perform local exploration and complex movements semi-independently while cooperating with visual input from the eyes.
Biochemist Peter Dews in 1959 tested learning in octopuses using a lever-pulling task. Individual octopuses bypassed the intended lever mechanics by attacking the apparatus, breaking the lever, and squirting jets of water at experimenters. Octopuses in laboratories in New Zealand and Germany repeatedly squirted water at overhead light bulbs to short-circuit the power supply because they disliked bright lights, forcing facilities to release them. A 2010 experiment confirmed giant Pacific octopuses can recognize individual humans wearing identical uniforms.
4. From White Noise to Consciousness
Subjective experience and consciousness are distinct categories. Sentience comes first in evolutionary history, while consciousness involves unified mental activities that arose much later.
Simona Ginsburg and Eva Jablonka suggest early subjective experience started as white noise. This inchoate buzz of metabolic electricity gradually became organized as nervous systems grew more complex.
The Evolution of Experience
Action and perception connect through causal arcs, meaning what you do affects what you sense next.
In tactile vision substitution systems, blind wearers feel vibrations on their back from a video camera, but they experience it as an external object moving in space only when they control the camera's movement.
Movement creates sensory feedback that can overwhelm an organism, forcing animals to evolve mechanisms to cancel out self-generated effects. Electric fish send out a command copy to their sensing system to counteract self-produced electric pulses, and earthworms cancel out self-produced touches to move forward.
Many animals keep information separated between different brain regions. In a study of nine birds, eight pigeons trained with one masked eye showed no inter-ocular transfer of the learned skill to the other side.
Visual processing splits into two distinct streams. The ventral stream handles categorization and conscious experience, while the dorsal stream handles unconscious real-time navigation.
Following carbon monoxide poisoning in 1988, patient DF lost her ventral stream and felt almost blind, yet she could still reliably post letters through a slot of varying angles using her dorsal stream.
Flexible pain-related behaviors indicate that pain is an old form of subjective experience. Hermit crabs given electric shocks are more reluctant to leave higher-quality shells and will tolerate shocks more when a predator's odor is present.
The Case of the Octopus
Subjective experience began as an inchoate buzz before organizing through sensorimotor loops, with octopuses developing advanced perceptual constancies.
Octopuses exhibit advanced perceptual constancies despite their unique evolutionary path. In 1956, animals trained to approach specific squares correctly chose the real size of a square even when it was presented at half the usual distance.
The octopus represents a hybrid system of agency due to delegated autonomy in the arms. The central brain shares control with peripheral networks, blurring the boundary between self and non-self.
In an experiment by Jean Alupay, octopuses subjected to crushed arms amputated them in some cases and tended and guarded the injured site.
5. Making Colors and Communicating
Giant cuttlefish grow up to three feet long and feature an octopus-like head with eight flexible arms and two feeding tentacles. A researcher named Alexandra Schnell noted that giant cuttlefish in captivity sometimes ambush visitors with well-aimed squirts of water. They possess large brains relative to their body mass and move via fin undulation or jet propulsion.
Cephalopod skin acts as a layered screen controlled directly by the brain, combining pigment-filled chromatophores with lower layers of reflecting cells to produce dynamic color patterns.
The skin features an outer dermis, followed by chromatophores. These are tiny sacs of colored chemicals attached to brain-controlled muscles that stretch or relax to show red, yellow, or black and brown pigments. Beneath these lie iridophores and leucophores, which are reflecting cells that bounce and filter incoming light to produce blues, greens, and whites. A giant cuttlefish holds approximately ten million chromatophores, forming a ten-megapixel screen. The author observed a large cuttlefish displaying a passing cloud on one side while the other side remained still and camouflaged.
Layered Skin and Light Sensing
Although physiological and behavioral tests suggest cephalopods have only one type of photoreceptor and are color-blind, research by Lydia Mäthger, Steven Roberts, Roger Hanlon, Desmond Ramirez, and Todd Oakley revealed that photoreceptor genes are active in the skin of cephalopods. In 2010, Mäthger, Roberts, and Hanlon published their paper on skin photoreceptors. Ramirez and Oakley published research showing that photoreceptor genes are active in the skin of Octopus bimaculoides and that detached skin can sense light and change chromatophore shape. Skin can sense light and respond independently of the brain, and the movement of chromatophores above light sensors could act as color filters, allowing a monochrome system to perceive color.
Individual giant cuttlefish exhibit distinct personalities, unique color repertoires, and specific interaction styles ranging from curious friendliness to intense hostility. A friendly cuttlefish named Matisse would suddenly explode into bright yellow across his entire body in less than a second. Another individual named Kandinsky maintained an extravagant home den twelve feet down, observed for about a week in 2009, featuring complex arm postures and red-orange flaring patterns. Conversely, some large males exhibited fierce territorial hostility with murderous-looking displays involving horns, hooks, and armor-like skin-folds.
Many low-level color changes in giant cuttlefish are not functional signals or camouflage, but rather inadvertent expressions of internal electrochemical activity. The author spent forty minutes observing the quiet cuttlefish symphony of a medium-size cuttlefish under a ledge whose skin cycled through an intricate symphony of rusts, grays, and greens while he remained completely still.
Baboons and Squids
Cephalopods and baboons represent an evolutionary asymmetry in communication, with cephalopods featuring complex signal production but simple social interpretation, while baboons have simple calls but complex narrative interpretation. Studied by Dorothy Cheney and Robert Seyfarth, baboons live in troops of eighty individuals with strict hierarchies and use only three or four calls, yet process them narratively to track social changes. Conversely, Caribbean reef squid, documented by Martin Moynihan and Arcadio Rodaniche, produce complex visual displays numbering around thirty ritualized displays, yet their social interactions and signal interpretations are far less complex. Moynihan and Rodaniche documented about thirty ritualized displays in Caribbean reef squid, suggesting they possessed a visual language with a grammar.
6. Our Minds and Others
Human thought relies on internalized language loops and global workspaces, representing a second major internalization in cognitive evolution.
In 1739, David Hume inspected his own mind and found no stable being. He concluded that you are merely a bundle of momentary images, passions, and impressions acting like mental atoms, inspired by Isaac Newton's physics.
Lev Vygotsky posited that complex human thought develops through the internalization of ordinary spoken language into a structured inner monologue. Vygotsky worked in the Soviet Union during the early twentieth century around the time of the Russian Revolution of 1917, suffering a crisis in 1930 before he died at age 37 in 1934. An English translation of his work Thought and Language appeared in 1962, and Merlin Donald published Origins of the Modern Mind in 1991.
Language and inner speech are not strictly essential for carrying out complex thought and internal information processing.
André Roch Lecours and Yves Joanette published a paper in 1980 describing Brother John, a French Canadian monk who experienced temporary attacks of severe aphasia causing total loss of speech and comprehension. He remained conscious during these episodes and managed to navigate practical tasks using gestures.
Inner Speech and Efference Copies
An efference copy is a neural command duplicate sent to perceptual areas to help the brain distinguish between sensory changes caused by its own actions and changes originating externally. When you decide to act, a faint copy of the motor command goes to perceptual regions so you can compensate for self-generated motions.
You compensate for eye movements so that the surrounding visual world is not perceived as shifting every time the head moves.
Inner speech likely originated as an exaptation of efference copy mechanisms used to control and monitor complex vocal actions. Daniel Dennett described this cognitive wiring as a Joycean machine in the head. In a 2001 headphone noise experiment, people mistook auditory imagination for real sounds.
Alan Baddeley and Graham Hitch developed their working memory model in the 1970s. Working memory relies on distinct subsystems:
- a phonological loop for imagined sounds;
- a visuospatial sketchpad for manipulating shapes.
Conscious thought operates by broadcasting information throughout a global network in the brain, allowing disparate mental contents to be integrated for novel tasks. French neurobiologists Stanislas Dehaene and Lionel Naccache defended their version of the workspace theory in 2001.
Full Circle
Cognitive evolution is bookmarked by two major internalizations where communication channels between organisms were turned inward to coordinate internal processes. German physiologists Erich von Holst and Horst Mittelstaedt introduced their framework on reafference and loops in 1950.
Cephalopods lack the complex internal feedback loops characteristic of human language because their skin display communications operate primarily as a one-way street. Because octopuses and squids cannot easily view their own chromatophore color and pattern changes on their skin in the way humans hear their own speech, their expressive displays are not embedded in rich efference-copy loops.
7. Experience Compressed and Senescence
Despite their large brains and complex intelligence, giant cuttlefish and octopuses have exceptionally short lifespans of only one to two years, while the giant Pacific octopus reaches a maximum lifespan of four years. You might wonder why animals invest heavily in expensive neural machinery for learning when they have almost no time to use it.
The author observed giant cuttlefish in the sea starting around 2008, initially assuming they were long-lived and experienced, only to realize that after a single breeding season they rapidly fall apart, lose their skin and arms, and die.
The Evolutionary Logic of Aging
The aging and death of animals cannot be explained simply as bodies wearing out like automobiles, because living bodies are composed of cells that continually divide and replace themselves. Aging evolves because natural selection weeds out late-acting harmful genetic mutations less efficiently than early-acting ones, since most individuals die from external dangers before old age.
Peter Medawar made the first step of the argument in the 1940s, George Williams added the second step in the 1950s, and William Hamilton put the theory into rigorous mathematical form in the 1960s. Natural selection favors genetic mutations that provide benefits early in life even if they carry harmful consequences later, because individuals are unlikely to survive to experience the late-stage costs.
Long and Short Lives
Animals adopt either semelparous or iteroparous reproductive strategies depending on external predation risks and whether the adult stage is dangerous. The ancestral abandonment of the protective external shell set cephalopods on an evolutionary path combining unbounded bodily flexibility, complex nervous systems, high vulnerability, and compressed lifespans.
Female octopuses are extreme semelparous organisms that settle into a den, tend a large clutch of thousands of eggs until they hatch, and die shortly afterward.
In 2007, a marine research unit at Monterey Bay inspected a deep-sea octopus nearly a mile underwater that successfully brooded her eggs out in the open for fifty-three months. This deep-sea octopus species breaks the normal cephalopod short-life pattern by living and brooding its eggs in cold water for over four years due to lower predation pressure. This represents the longest egg-brooding period reported for any animal species, leading to an estimated potential lifespan of sixteen years based on brooding fractions.
8. Octopolis and the Future of Oceans
Field discoveries at sites like Octopolis prove that octopuses engage in complex social behaviors when provided with stable shelter.
In 2009, Matt Lawrence discovered Octopolis at a depth of 50 feet below the surface off the east coast of Australia, where over a dozen octopuses gather in a small arena. Unmanned GoPro cameras and observations by researchers show that octopuses engage in frequent interactions, including arm-probing and policing behaviors, rather than living entirely solitary lives.
In January 2015, researchers recorded an unprecedented level of activity where a large male octopus continually policed the site, chasing off rivals and herding females.
Ecosystem Engineering
Octopuses act as ecosystem engineering agents by collecting food and discarding shells. This activity builds an artificial reef that transforms the physical environment and attracts other marine species.
The site was likely seeded by a dropped metal object on a fine sand bottom. Octopuses brought back scallops to eat, and the accumulating shell debris enabled the construction of stable dens up to 40 centimeters deep. This positive feedback loop attracted higher concentrations of fish, sharks, rays, and squid compared to surrounding areas.
Parallel Brain Evolution
Genetic evidence suggests that complex nervous systems and high intelligence evolved at least twice independently within cephalopods. The split between octopuses and decapods occurred 270 million years ago in the Permian period, significantly earlier than the previous fossil-based estimate of 170 million years ago. Furthermore, protocadherin molecules used to build nervous systems expanded separately in squid and octopuses, indicating multiple parallel paths of brain evolution.
Christelle Jozet-Alves and her team in Normandy studied episodic-like memory in cuttlefish, demonstrating advanced cognition on the decapod branch.
Human impacts on the oceans accumulate as unseen environmental stresses until ecosystems reach a critical tipping point and experience sudden collapse. Thomas Huxley predicted in an 1883 speech that major sea fisheries like cod and herring were inexhaustible, but oceans now face severe pressures from acidification and expanding dead zones.
10 Key Ideas
- The most recent common ancestor shared by mammals and cephalopods existed roughly 600 million years ago and was likely a small, flattened worm-like creature.
- Nervous systems likely evolved for internal physical coordination rather than mere sensory-motor links, sparking a Cambrian arms race.
- By abandoning their external shells, cephalopods gained immense bodily freedom while distributing most of their neurons directly into their arms.
- Subjective experience began as an inchoate buzz before organizing through sensorimotor loops, with octopuses developing advanced perceptual constancies.
- Cephalopod skin acts as a layered screen controlled directly by the brain, combining pigment-filled chromatophores with lower layers of reflecting cells to produce dynamic color patterns.
- Human thought relies on internalized language loops and global workspaces, representing a second major internalization in cognitive evolution.
- Field discoveries at sites like Octopolis prove that octopuses engage in complex social behaviors when provided with stable shelter.