Our Senses: An Immersive Experience - Rob DeSalle 2018

The Brainless Majority: Sensing the Environment in Organisms without Brains

“Plants don’t have a brain because they are not going anywhere.”

—Robert Sylwester, professor of education and philosopher

Our brain and our senses are the products of an experiment, billions of years old, that has occurred on our planet. Sorting out which events matter in that experiment for us to understand our unique capacities for perceiving the world around us requires an evolutionary approach. And that approach requires us to focus on a couple of important outcomes of evolution: biodiversity and exceptions. An amazing diversity of organisms have existed over the 3.5 billion years that organismal life has evolved on Earth. Without this diversity, we could not examine many nuances of our own sensory capacity. Our ability to hear sounds in a specific range, for example, is well described, but we would not know that our auditory range is biologically limited without our knowledge of how bats echolocate. So, an exploration of biodiversity puts our own biological characteristics involved in sensing into perspective. Exceptions in nature draw our attention to the nitty-gritty of how nature works and allow us to question why they occur. Examples of exceptional sensing come both from nature and from the record of human sensory limits. Many exceptions have evolved relative to our lineage. Some of these sensory exceptions help us understand how a particular sense works as well as how a sensory response might have evolved.

One example of this utility of sensory exceptions is how olfactory genes in animals are distributed. The number of functional olfactory genes found in vertebrates so far ranges from fewer than twenty in the green anole, a small lizard, to more than two thousand in the elephant. By comparison, humans have a respectable four hundred or so olfactory genes. If we couple these gene numbers with how different animals smell, we can learn a lot about our olfactory sense. The diversity of organisms on this planet reveals amazing natural experiments and offers great explanatory power with respect to understanding the senses.

All species are related through common ancestry, and this allows us to look at the steps that might be involved in the evolution of our unique sensory capacities. The tree of life is a superb way to demonstrate both the importance of biodiversity and the utility of common ancestry. For this reason, throughout this book I will use the tree of life as an organizing principle for our sensing organs and the organ that processes the sensory input (the brain).

The human brain, a most complex structure, is where our senses are processed and where perception exists. The brain evolved in higher animals to collect information from the outer world, to make sense of those data, and to promulgate survival. Most of the almost two million species that scientists have named and described to date have brains. (Scientists discriminate between the raw number of species that exist and the number of named species that are out there because they consider a species that has not been named or described as somewhat meaningless in an ordered world.) This number might lead one to think that we live in a very “brainy” world and, hence, one that is nicely tuned to the senses we’re familiar with. But the grand majority of the life on this planet do not have brains, and so not having a brain has also been quite successful with respect to survival. Organisms without a brain can nonetheless sense and interpret the environment they live in quite well. It turns out that these organisms without brains are a neglected majority.

Most organisms are single celled and still unknown to science. Recent work on the human microbiome reveals that, on average, more than ten thousand kinds of bacteria live on and in our bodies, many undescribed and unnamed taxonomically. And that’s just our bodies. When oceans and soil are examined, the number of bacterial species explodes. In the 1980s, the famous entomologist Terry Erwin suggested the stunning possibility that ten to a hundred times more species of organisms might live on Earth than the 1.5 million or so known at the time. Then scientists began to discover more and more novel species of bacteria. In 2009, microbiologist Rob Dunn theorized that there are at least one hundred million species of microbes (journalists called this Dunn’s Provocation), which suggests that at least two hundred million species of organisms are living on Earth. Most of these species are microbial and thus lack brains. To add to this brainless majority, consider that 99.9 percent of all the organisms that have ever lived on the planet have gone extinct. Given that bacteria and single-celled organisms existed for probably two billion years before animals and plants emerged, this makes the estimated number of single-celled organisms even more stunning. Organisms with brains are and always have been an extreme minority, making Earth a pretty brainless planet.

So why the fuss about brains? A brain isn’t required for perception. Galileo Galilei once wrote, “Before life came, especially higher forms of life, all was invisible and silent although the sun shone and the mountains toppled.” Galileo’s statement in retrospect means that before the bacterial mechanism for detecting light evolved, there was no perception of light as light and, hence, no light. The first organisms to evolve cellular mechanisms for detecting light metaphorically shouted, “Let there be light!” These first sensing organisms more than likely focused on one environmental stimulus, such as light, or on a specific kind of molecule floating around, or gravity, or magnetism.

Andriy Anishkin and colleagues theorize that the primordial sense was more than likely a response to mechanical stress on the lipid membrane surrounding a cell. In other words, any physical force that displaced the primordial membrane was the first external stimulus that cells learned to sense. Experiments reveal that force on the outer lipid membrane of a cell can result in conformational changes in the molecules that might be embedded in the membrane. Such changes in molecular conformation can act like switches in the embedded cells. If the molecules are squished or contorted, they will change shape, which could turn on or off other responses inside the cell. One common prevalent force that the outside environment enforces on a cell would be osmotic pressure caused by different salt concentrations inside and outside the cell. Anishkin and his collaborators suggest that forces like osmotic pressure outside primordial cells might have been the first sensory experiences that enclosed cellular life experienced. Indeed, the phenomenon still exists in modern cells and points to an evolutionary frugality over the 3.5 billion years of life on Earth. When a structure or process in evolution is found to be adaptive, it lives on in its descendants as a result of natural selection. But another interesting possibility is that unrelated organisms rediscover the process or structure over and over again in evolutionary history. Examples of this latter kind of evolution, called analogy or convergence, abound. Wings are a good example of convergence, having arisen independently in birds, mammals, insects, and pterosaurs.

The answer to the question posed earlier, “Why brains?” then, is that primordial single-celled organisms had extremely limited capacities to sense more than single environmental inputs, which meant that these organisms had very limited perceptions of their environments. Brains evolved to allow for more precise integration of sensory input and for more exquisite perception of the information from the environment. Brains make our environment more understandable by detecting and processing a wider range of the outer world stimuli that are continuously bombarding us.

Enormous amounts of chaotic information stream, float, and dart around any organism’s environment, confront its sensing organs, and have to be processed by a brain. One form of that chaos is best described as coming in waves. For the purpose of understanding how information from light enters our nervous system, we can say that electromagnetic radiation like light behaves both as a wave and as a particle. This means that light has qualities that waves and particles have. One characteristic of a wave is its length. Next time you are at the beach, watch the waves coming in. The wavelength is the distance from one wave’s peak to the next one’s peak. Electromagnetic radiation of different wavelengths (fig. 1.1) have different characteristics, and they can range from 0.000000000001 meters (gamma rays) to more than 10,000 meters (radio waves). Humans can detect light in only a very narrow range of this spectrum, from 400 to 700 nanometers, or 0.0000004 to 0.0000007 meters. The unseen (by human eyes) range of light outside the small end of the spectrum of wavelengths (400 nm) is what is called ultraviolet, or UV, light. Just outside the larger end of the spectrum (700 nm) is infrared, or IR, light. In between are the colors we see from smaller wavelengths to larger—violet, blue, green, yellow, orange, and red. How and why our color perception got stuck in this narrow range of wavelengths is a story about evolution and adaptation. To understand this, we need to understand the physics of light and wavelengths.

BOX 1.1 | WHY AND HOW DO WE SEE COLORS?

When light hits an object, it slams into a large number of molecules that make up the object. Since light and electromagnetic radiation are also considered particulates, researchers have given the fundamental particle of electromagnetic radiation a name—the photon. When it runs into something, a photon has two options: it can be either absorbed or reflected. So, when light (which consists of photons of varying wavelengths) hits an object, millions and millions of interactions are taking place. Some molecules will reflect the photons, and others will absorb them. The photons that are reflected then hit our eyes, giving color to an object. For instance, plant tissues contain a molecule called chlorophyll. Because of its shape and size (it looks a little like Thor’s hammer), this molecule absorbs light at 430 and 662 nanometers. These two wavelengths are where blue and red light, respectively, reside. So, chlorophyll does not absorb light between 430 and 662 nanometers, which is the wavelength for green light and a part of the color spectrum we see. The unabsorbed green light has only one place to go, and it is reflected off the plant. If a broad range of light hits an object that has ways of absorbing the different wavelengths, then the object absorbs all of those wavelengths. The object will have no photons bouncing off it in the visible range, and it will for all practical purposes have no color. The colors organisms detect, then, are simply the result of the reflection of light at different wavelengths to our eyes.

We don’t see the entire spectrum of light—say, into ultraviolet and infrared wavelength ranges and farther—because our eyes and the eyes of our ancestors evolved to detect only a narrow range of wavelengths. Although for most organisms the Sun is the major source of electromagnetic radiation, many other sources generate the photons that make up electromagnetic radiation. X-rays are an example of light created by the emission of electrons from atoms. Our eyes do not detect X-rays, but we have created a clever way of using photography to detect X-rays. This theme of humans inventing clever ways of expanding the range beyond our natural limits, not only with seeing but with many of the other senses, is an important and ongoing concept. Other sources of wavelengths include bioluminescence. This form of light is emitted in our visible range and results in spectacular instances of living organisms producing and not reflecting light.

Figure 1.1. The range of photons in wavelength that we are exposed to in nature. Light waves range over eighteen or so orders of magnitude. The visible part of light is only a small sliver between 400 and 700 nanometers.

Another part of the chaos is molecules in the air as well as in the solids, gases, and liquids with which we come into contact. These molecules consist of atoms that form complexes in many ways, creating a plethora of incredibly small objects floating in the air or in what we ingest. Some of these molecules are very small, but all have distinctive shapes and sizes and can be detected as unique through a lock-and-key mechanism implemented by proteins embedded in the cell’s membrane. Parts of these proteins flap continuously outside the cell and act as locks. When a small molecule comes along that fits the lock like a key, it forms a complex with the protein embedded in the membrane and changes the protein’s shape. This change initiates a set of reactions inside the cell, causing a chain reaction that changes the state of the cell. What happens in the cell is called signal transduction, and this process is at the base of how our nervous system works as well as how single-celled organisms react to external stimulation. These small molecules floating around in our environment are the basis for how we and other organisms taste and smell.

Sometimes the displacement of the air (or water if we are swimming) around us causes sensation. Think of when we use a hand dryer in a public restroom: we can feel the air being displaced by the blower on our hands. We can also feel, as anyone can attest, when our head comes into contact with something solid, such as a low beam in the basement. So, when our skin comes into contact with a gaseous, liquid, or solid object, we experience a mechanical reaction. Organisms also need to know where they are in space, so many life-forms have evolved ways of keeping track of their position, and this leads to balance. The chaos of environmental stimulation that causes the need for balance comes from gravity and from the organism’s movement. Other environmental variables include temperature, magnetic fields, and electrostatic fields.

BOX 1.2 | HOW DOES SOUND WORK?

Sounds are wavelength-based stimulations to our senses carried through water, air, gels, and other media as vibrations. Sound waves tend to displace air and other particles floating in the air. A range of sound exists because different sources can emit different wavelengths. As with light, organisms on this planet have evolved to detect sound waves in a narrow range relative to the overall range of sound. Sound waves travel in cycles that go from one wave peak to the next. The lower the number of cycles per unit of time, the lower the sound will be. The higher the number of cycles, the higher the sound will be. The unit for sound is called a hertz, and it measures the number of cycles per second of a sound wave. Humans can hear sound over a range of three magnitudes of hertz (from 20 Hz to 20,000 Hz), but other animals on the planet can hear sounds that are lower and higher.

Specialized cells in an organism detect sensory information from the environment, but how do they do this? The mechanism for single-celled organisms is very different from that of such multicellular organisms as plants and higher animals. In higher animals, brains process the information received from the sense organs.

Even those lineages of the single-celled organisms that we call bacteria and archaea can sense aspects of the world around them. This is because the environment comes into contact with things around these tiny organisms all the time. One need only view videos of predatory bacteria eating prey bacteria to realize that sensing is taking place. As the predators begin to decimate the prey, it’s stunning how rapidly the prey bacteria selectively disappear. Here, a sensing of “You are my species, I’ll leave you alone . . . and you aren’t, so therefore you are good to eat,” is being accomplished very efficiently. Even more impressive are videos of single-celled eukaryotes chasing and engulfing other single-celled organisms. But to me the most impressive video of bacteria sensing the external world is one showing “line-dancing” microbes that respond to magnetism as described below.

Some bacteria can count, and this capacity requires that the counting cell sense its surroundings. Quorum sensing is perhaps one of the most primitive ways cells sense and communicate with each other. But the basic theme of using molecules to communicate sense permeates all life on earth. Just as the quorum-sensing mechanism is based on molecular interactions, so are the senses of so-called more complex organisms. Single-celled organisms have a molecular system for detecting light, and some microbes (and indeed more complex animals) can sense magnetic fields. Magnetotactic bacteria orient themselves along the Earth’s magnetic field because their cell membranes contain small particles of iron sulfide or magnetite (magnetosomes) encased in a membranelike organelle, and they line up in this encasement. Even though these tiny particles are lined up, more is needed for the line dancing to occur. The aligned magnetosomes within the bacteria are arranged in parallel, giving the bacteria a dipole characteristic and transforming them into tiny magnets with magnetic poles. Many species of bacteria are magnetotactic. The phenomenon apparently evolved just once in the evolutionary history of microbes, because most magnetotactic bacteria are in the phylum Proteobacteria and two other closely related phyla. In addition, the genes that modulate the construction of this organelle are found clustered in the genomes of magnetotactic bacteria, leading to two interesting aspects of the evolution of the phenomenon.

First, the tight clustering of the genes involved in making up the magnetosomes and the organelle that contains them indicates a single mechanism for the phenomenon (at least in the phyla where magnetotactic bacteria are found). Second, the genes are located on what is called a colonization island of DNA that can move around horizontally to other species. This horizontal transfer could implement and speed up the evolution of the magnetotactic trait in other bacteria.

In the absence of an interfering magnetic field, the bacteria align with the Earth’s magnetic field. Why would a microbe care about this? Because it craves nutrients for survival, and knowing the direction of this magnetic field helps it seek out more nutrient-rich environments suited to its biology. For instance, microbes in the phyla where magnetotactic bacteria reside crave to be in a sweet spot in environments called the OAI, or the oxic (oxygen-rich)—anoxic (oxygen-absent) interface, as well as in anoxic areas very near to the OAI. They have evolved to prefer this environment, and because they have strong flagella that can propel them, they are on the lookout for such environments. It turns out that, because of the curvature of the Earth, not only does the Earth’s magnetic field point north-south, but it also points at an angle to the surface. The angle to the Earth’s surface allows orientation from surface to below surface. Being able to sense the Earth’s magnetic field in the surface-to-below-surface direction allows magnetotactic bacteria to travel the most efficient path to the OAI, because the OAI is away from the surface.

BOX 1.3 | QUORUM SENSING

Microbes often need to sense the density of their populations to respond to environmental challenges. The classic example of this kind of sensing, called quorum sensing, is found in Aliivibrio fischeri, a bioluminescent bacterium that resides in the light-producing organ of the Hawaiian bobtail squid (Euprymna scolopes). The squid and the bacteria have a mutualistic relationship whereby the squid cultures the A. fischeri while the bacteria light up the squid’s light organ, which the squid uses to camouflage itself from predators. But the bacteria need to know when to light up, because it would be a terrible waste of energy to stay lit up all of the time. And so a mechanism for regulating the expression of bioluminescent-producing proteins has evolved in the squid light organ that uses a clever capacity of the bacteria to sense their population size. The bacteria produce a protein called an inducer, which they recognize by another protein they produce called a receptor. When the inducer and the receptor bind to each other through (a lock-and-key mechanism), a cascade of genes in the bacterial genome is turned on, and a bioluminescent reaction occurs. When only a small number of A. fischeri are present in the light organ, the inducer is so dilute that it effectively does not bind the receptor, and no light is produced. This kind of sensing is entirely molecular.

What happens when the microbes are tricked into responding to magnetic fields other than the Earth’s? Researchers at the Korean Institute of Science and Technology have built a tiny apparatus using a petri dish on a platform where a magnetic field is created below the dish. The magnetic device can be rotated with controls so that it overcomes the Earth’s magnetic field and overtakes the behavior of the bacteria. Magnetotactic bacteria are placed into the petri dish, and the magnetic field is rotated with a dial by the “line-dance caller” in the lab—apparently to the tune of “Cotton-Eyed Joe.” The magnetotactic bacteria respond with a decent version of line-dancing moves, by rotating in unison from left to right and forward to backward. The images of single-celled organisms dancing, and dancing well, are therefore quite humbling to a poor dancer like myself. Dancing is, of course, used as a metaphor in this instance, and it is important to recognize the metaphor for what it is.

Single cells need to know where they are in space and what they come into contact with and when. Since sunlight was a pervasive environmental factor billions of years ago, some bacteria also needed to know where light was and indeed used light as a means by which to live. So single cells developed fairly intricate and efficient ways of detecting external factors such as gravity, light, and environmental chemicals. Andriy Anishkin and his colleagues have proposed that tactile sensing in the original sense (as they call it) is a good argument for this being the first and perhaps most important sense a cell can have. But the order in which cells and organisms developed other senses would have to be speculation. We can, on the other hand, come up with pretty sound mechanisms as to why and how a cell might have developed a particular way of sensing.

Some bacteria use light as “food,” just as plants do. One large group of bacteria that do this is the cyanobacteria. Molecules can interact with light by absorbing photons of light, and this is how these bacteria obtain light as a living. The mechanisms for using light as food in both plants and bacteria are practically the same. This observation at first glance is kind of wild. Bacteria and plants are not closely related, and there is no clear ancestor-descendant reason why plants should have a characteristic that bacteria have until one considers the origin of the chloroplast, which is the organelle in plants that converts light into nutrition for plant cells. The chloroplast in plants is actually the remnant of an ancient cyanobacterium that was engulfed by the ancestral plant cell. The symbiosis caused by the engulfed cyanobacteria in plant cells was such a lifestyle improvement for the ancestral plant cell that it stuck in an evolutionary context and is now a mainstay of plant life on the planet. The history of engulfment events by early eukaryotic cells of various kinds of bacteria is complex and sometimes convoluted. Some plant cells have engulfed other cells multiple times, and even multiply engulfed cells have been engulfed.

Another way that bacteria have exploited light is through altering the molecular properties of a class of molecules called opsins. These molecules are embedded in cell membranes where photons of light can hit them. Opsins have smaller molecules called chromophores latched to their inner structures. The chromophore clinging to the innards of the opsin forces the bigger molecule into a specific nonactive state while it lies embedded in the cell membrane. When light of a specific wavelength hits the cell, it also strikes the chromophore and causes it to be displaced, and the structure of the opsin itself changes, triggering other reactions in the cell.

In some single-celled bacteria, there is a molecule called rhodopsin embedded in the cell membrane that reacts with light. But unlike more complex organisms, the bacterial rhodopsin acts like a pump that brings high concentrations of chloride or moves protons into the cell that in turn changes the way the cell carries on its life. Single-celled eukaryotes also have rhodopsins that react when hit with light. The bacterial rhodopsin is pretty different from higher eukaryotic opsins, so whether or not the vertebrate opsins are derived from bacterial rhodopsin is not established. The point here is that the mechanisms for how opsins and rhodopsins detect light are similar and offer a preview to how higher animals sense light. Another point is that in single-celled organisms the mechanisms are carried out by proteins without a centralized need for processing the information in a brain. The “decisions” a single-celled organism makes as a result of environmental stimulus are rapid, chemical, and internal to the single cell. Higher organisms receive the environmental stimulation in ways very similar to single-celled organisms but do the processing of the subsequent information quite differently.

Multicellular life diverged from a single-celled ancestor about 1.5 billion years ago. A large number of single-celled eukaryotes exist today, and the patterns of their relatedness make it clear that there were many early events of divergence for single-celled eukaryotes into multicelled animals and plants. This observation holds because not all single-celled eukaryotes are each other’s closest relatives and not all multicellular organisms come from the same common ancestor. Some single-celled eukaryotes, for example, are more closely related to plants than they are to other single-celled eukaryotes. For instance, the single-celled eukaryotes known as Clamydomonas (affectionately called Chlamy by people who study them) and algae are single-celled eukaryotes that are more closely related to plants than they are to other single-celled organisms like amoeba.

Plants can communicate the stimulus of the surrounding world to themselves quite well but have evolved very different mechanisms for doing this than animals. An excellent example is a sunflower: if you can, spend a few hours watching one respond to sunlight. Actually, the most interesting response the sunflower has to light occurs just before sunrise, when the plant’s flower slowly turns toward where it anticipates the Sun will rise. The sunflower is pretty good at moving its floret and is very good at the timing. Another example is the mimosa, a plant that responds very rapidly to touch, and anyone who has seen Little Shop of Horrors should be immediately reminded of a Venus flytrap, which responds rapidly and voraciously to prey items that unwittingly wander across its trapping apparatus (fig. 1.2). Plants, however, do not have nerve cells and hence do not have a brain or a nervous system like animals. (I make these statements about plants and nervous systems even though a journal called Plant Neurobiology exists and even though several institutes are dedicated to the study of the neurobiology of plants. The focus of plant neurobiology is not the same as animal neurobiology.)

Metaphor has become important in the comparison of how organisms respond to the environment. An organism with a “metaphorical brain” like a plant does not process information from the external world the same way vertebrates do, but this is not surprising. By metaphorical brain, I mean a system that is analogous to a vertebrate brain but not at all neural. This capacity to respond to the outside world is what prompted some researchers to initiate the plant neurobiology approach. But it is very difficult to deny that plants don’t have brains and they don’t have nervous systems. I prefer to acknowledge that plants are pretty good at sensing the outer world and have some way of centralizing their sensing of the outer world, but in a functional structural context, they do not have brains. In evolutionary biology, we might say that the plant version of a nervous system has converged on the insect or vertebrate brain. The plant’s central sensing system is a metaphor for the invertebrate or vertebrate nervous system. It is intellectually much more pleasing to me to realize that plants have figured out a novel way to perceive the outer world that has nothing to do with a nervous system. And indeed, when we start to examine the ways that animals with nervous systems have evolved structures and mechanisms for the traditional senses, this theme is repeatedly borne out. So as Michael Pollan, the outspoken defender of plant life on this planet, suggests, perhaps we should call it, not “plant neurobiology,” but rather “plant intelligent behavior.” And in this context, plants have evolved intelligent behavior without any reference or evolutionary similarity to the animal way of getting at intelligent behavior, other than using some of the very basic molecular tools in the evolutionary toolbox that most multicellular eukaryotes have. This intelligent behavior allows the plant to sense stimuli from the environment such as light or chemical concentrations and to interpret them in an “intelligent” manner. The neural basis of plant intelligent behavior is simply another solution to cell-to-cell communication that life on Earth has discovered and evolved as a response to the need for sensory connection to the outer world.

Figure 1.2. An example of plant neurobiology or plant intelligent behavior? The Venus flytrap (Dionaea muscipula).

It is no surprise that organisms without eyes, ears, noses, skin, and mouths can’t see, hear, smell, touch, and taste. These so-called traditional or Aristotelian senses are the bailiwick of advanced animals. And so organisms without these attributes have focused their sensing on other environmental stimuli, like electrical and magnetic fields and chemical signals that don’t behave like taste and smell. Organisms that can see, hear, smell, touch, and taste have evolved an amazing array of anatomical and physiological traits that enhance those senses. The breadth of mechanisms that life has evolved to sense the outer world of environmental stimuli is stunning.