The Meaning of Human Existence

by Edward O. Wilson

  Why did an outwardly arcane topic of theoretical biology excite such fierce partisanship? Because the problem it addresses is of fundamental importance, and the stakes in trying to solve it had become exceptionally high. Furthermore, inclusive fitness was beginning to resemble a house of cards. To pull even one out risked collapsing the whole. Pulling cards, however, was worth the price to reputation. There existed in the air the promise of a paradigm shift, a rare event in evolutionary biology.

  In 2010, the dominance of inclusive fitness theory was finally broken. After struggling as a member of the small but still muted contrarian school for a decade, I joined two Harvard mathematicians and theoretical biologists, Martin Nowak and Corina Tarnita, for a top-to-bottom analysis of inclusive fitness. Nowak and Tarnita had independently discovered that the foundational assumptions of inclusive fitness theory were unsound, while I had demonstrated that the field data used to support the theory could be explained equally well, or better, with direct natural selection—as in the sex-allocation case of ants just described.

  Our joint report was published on August 26, 2010, as the cover article of the prestigious journal Nature. Knowing the controversy involved, the Nature editors had proceeded with unusual caution. One of them familiar with the subject and the mode of mathematical analysis came from London to Harvard to hold a special meeting with Nowak, Tarnita, and myself. He approved, and the manuscript was next examined by three anonymous experts. Its appearance, as we expected, caused a Vesuvian explosion of protest—the kind cherished by journalists. No fewer than 137 biologists committed to inclusive fitness theory in their research or teaching signed a protest in a Nature article published the following year. When I repeated part of my argument as a chapter in the 2012 book The Social Conquest of Earth, Richard Dawkins responded with the indignant fervor of a true believer. In his review for the British magazine Prospect, he urged others not to read what I had written, but instead to cast the entire book away, “with great force,” no less.

  Yet no one since that time has refuted the mathematical analysis by Nowak and Tarnita, or my argument favoring the standard theory over inclusive fitness theory in the interpretation of field data.

  In 2013 Nowak and I were joined by another mathematical biologist, Benjamin Allen, in a still deeper expansion of the ongoing analysis. (Tarnita had moved to Princeton, where she was busy adding field research to her mathematical modeling.) In late 2013 we published the first in a planned series of refereed articles. Because of the need for exactitude, and the material that these articles contain that may be relevant to the history and philosophy of the subject, I’ve taken the step of providing a simplified summary of the first one in the appendix of this book.

  Now at last we can return to a key question in a more open spirit of inquiry: What was the driving force in the origin of human social behavior? The prehumans of Africa approached the threshold of advanced social organization in a manner parallel to that in the lower animals but attained it in a very different manner. As brain size more than doubled, the bands used intelligence based on vastly improved memory. Where primitively social insects evolved division of labor with narrow instincts that play upon categories of social organization in each group, such as larvae and adults, nurses and foragers, the earliest humans operated with variable instinct-driven behavior that made use of detailed knowledge of each group member by all the others.

  The creation of groups from personal and intimate mutual knowledge was the unique achievement of humanity. While similarity of genomes by kinship was an inevitable consequence of group formation, kin selection was not the cause. The extreme limitations of kin selection and the phantom-like properties of inclusive fitness apply equally to humans and to eusocial insects and other animals. The origin of the human condition is best explained by the natural selection for social interaction—the inherited propensities to communicate, recognize, evaluate, bond, cooperate, compete, and from all these the deep warm pleasure of belonging to your own special group. Social intelligence enhanced by group selection made Homo sapiens the first fully dominant species in Earth’s history.

  III

  OTHER WORLDS

  THE MEANING OF HUMAN EXISTENCE IS BEST

  UNDERSTOOD IN PERSPECTIVE, BY COMPARING

  OUR SPECIES WITH OTHER CONCEIVABLE LIFE-

  FORMS AND, BY DEDUCTION, EVEN THOSE THAT

  MIGHT EXIST OUTSIDE THE SOLAR SYSTEM.

  7

  Humanity Lost in a Pheromone World

  Let’s continue this journey in a new direction. The greatest contribution that science can make to the humanities is to demonstrate how bizarre we are as a species, and why. The effort to do so is part of research on the natures of all the other species on Earth, each bizarre in its own way. We can go so far as to anticipate a bit the properties of life on other planets, including those that may have evolved human-grade intelligence.

  The humanities treat the strange properties of human nature by taking them as “just is.” With this perception as a bedrock, creative artists spin stories, make music, and create images in endless detail. The traits that define our species diagnostically appear very narrow when put against the full backdrop of biodiversity. The meaning of human existence cannot be explained until “just is” is replaced with “just is, because.”

  Let us begin then with the picture of how very specialized and peculiar is our beloved species among the legions of different life-forms that compose Earth’s biosphere.

  It was only after eons of time, during which millions of species had come and gone, that one of the lineages, the direct antecedents of Homo sapiens, won the grand lottery of evolution. The payout was civilization based on symbolic language, and culture, and from these a gargantuan power to extract the nonrenewable resources of the planet—while cheerfully exterminating our fellow species. The winning combination was a randomly acquired mix of preadaptations, which include a life cycle spent entirely on the land, a large brain and the cranial capacity to evolve a still larger brain, free fingers supple enough to manipulate objects, and (this is the hardest part to understand) reliance on sight and sound for orientation instead of smell and taste.

  Of course we think ourselves brilliant in our ability to detect chemicals with nose, tongue, and palate. We proudly recognize the bouquet arising from the swirl and aftertaste of a fine vintage. We can identify a darkened room at home from its signature odor alone. Yet we are chemosensory idiots. By comparison most other organisms are geniuses. More than 99 percent of the species of animals, plants, fungi, and microbes rely exclusively or almost exclusively on a selection of chemicals (pheromones) to communicate with members of the same species. They also distinguish other chemicals (allomones) to recognize different species of potential prey, predators, and symbiotic partners.

  What we enjoy as the sounds of nature are also a small slice of the potential. Bird songs stand out, of course, but bear in mind that birds are among the very few creatures that share our dependence for communication on audiovisual channels. Their utterances are joined by the croaking of frogs, chirping of crickets, and shrilling of katydids and cicadas. Add if you wish the twilight chittering of bats, although these calls, used for the echolocation of obstacles and flying prey, have a pitch above our range of hearing.

  Our limited chemosensory skills have profound implications for our relation to the rest of life. So on the side I feel obligated to ask, if flies and scorpions sang as sweetly as songbirds, might we dislike them less?

  Turning to the visual signals of animal communication, we enjoy the dances and body coloration of birds, fishes, and butterflies. There are also the brilliant colors and displays of insects, frogs, and snakes used to warn off would-be predators. The messages are urgent and not intended for the delectation of the predators, but instead say, “If you eat me you will die, or get sick, or at least you will hate the taste.” Naturalists have a rule about these warnings. If an animal is beautiful and also appears indifferent to your close approach, it is not m
erely venomous but probably even deadly. Examples include slow-moving coral snakes and insouciant poison-dart frogs. We can see this much, and both enjoy and survive, but we cannot see ultraviolet, with which many insects order their lives—butterflies, for example, in search of ultraviolet-radiating flowers.

  The audiovisual signals of the living world excite our emotions and throughout history have often inspired great creative works, the best of music, dance, literature, and the visual arts. They are nevertheless of themselves all paltry compared to what goes on around us in the world of pheromones and allomones. To illustrate this humbling principle of biology, imagine that you had the power to see these chemicals as vividly as the rest of life all around you that smells them.

  You are thrust instantly into a world far more dense, complex, and fast-moving than the one you left behind or even imagined. This is the real world of Earth’s majority biosphere. Other organisms live in it, but until now you have only lived on the edge. Billowing clouds lift off the ground and vegetation. Odorant tendrils leak out from beneath your feet. Breezes pull all this up past the tops of the trees, where in the stronger winds the tendrils are quickly torn apart and dissipate. Below the ground, confined by litter and soil, wisps arise from rootlets and fungal hyphae, then seep through nearby crevices. The combinations of odors vary from site to site, separated at distances as short as a millimeter away. They form patterns and serve as guideposts—used by ants and other small invertebrates all the time but beyond your meager capacity as a human. In the midst of the background odor field, rare and unusual organic chemicals flow in ellipsoidal streams and expand in hemispherical bubbles. These are the chemical messages emitted by thousands of species of small organisms. Some are produced as effluents evaporating off their bodies. These serve predators as a guide to prey, and equally they serve prey as a warning of approaching predators. Some are messages to others of the same species. “I’m here,” they whisper to potential mates and symbiotic partners. “Come, come, please come to me.” To potential competitors of the same species, like the pheromones deposited by dogs onto fireplugs, they warn, “You’re in my territory. Get out!”

  Researchers over the past half century (I had a wonderful time as one of them during the early years, working on communication in ants) have discovered that pheromones are not just broadcast into the air and water for others to pick up. Instead they are aimed with precision at specific targets. The key to understanding any pheromonal communication is the “active space.” Whenever odor molecules drift outward from their source (most commonly from a gland in the body of an animal or other organism), a concentration remains within the center of the plume produced that is high enough to be detected by other organisms of the same species. To a remarkable degree, the evolution of each species over thousands or millions of years has engineered the size and structure of the molecule, as well as the amount released in each message, and finally the sensitivity of smell to it in the receiving organism.

  Consider a female moth summoning males of her species in the night air. The nearest available male may be a kilometer away—the equivalent of about fifty miles when converted from moth body length to human body length. As a consequence the sex pheromone must be powerful, and so it has proved in real cases studied by pheromone researchers. A male Indian meal moth, for example, is stirred to action by as few as 1.3 million molecules per cubic centimeter. You might think that is a lot of pheromone, but it is actually a vanishingly small amount when compared with, say, a gram of ammonia (NH3), which contains 1023 molecules (one hundred billion trillion) molecules. The pheromone molecule needs to be not only powerful to attract the right kind of male, but also of some rare structure or other, making it highly unlikely to attract a male of the wrong species—or worse, a moth-eating predator. So precise are some sex attractants of moths that those of closely related species differ only by a single atom, or possession or location of a double bond, or even just an isomer.

  The male moth of species with such a high level of exclusivity faces a severe problem in finding a mate. The ghostlike active space he must enter and follow starts at a pinpoint on the female’s body. It proceeds as a roughly ellipsoid (spindle-shaped) entity until it finally dribbles out to a second pinpoint, then disappears. In most cases the male cannot find the target female by simply moving from a weak concentration of odor along a gradient of ever-increasing concentration, as we do when sniffing out the source of a hidden kitchen smell. It uses another, but at least equally effective method. Upon encountering the pheromone plume the male flies upwind until he reaches the calling female. If he loses the active space, which can happen easily as a breeze shifts and warps the odor stream, he zigzags from side to side through the air until he enters the active space again.

  The same magnitude of olfactory power this requires is commonplace throughout the living world. Male rattlesnakes find willing females by following pheromone tracks. Both sexes, their tongues flicking in and out to smell the ground, close in on a chipmunk with no less the precision of a hunter tracking a mallard duck with the barrel of his gun.

  The same degree of olfactory skill exists anywhere in the animal kingdom whenever there is a need to make fine discriminations. Among mammals, including human beings, mothers can distinguish the odor of their own infants from those of others. Ants can separate nestmates from aliens in tenths of a second with sweeps of their two antennae over the bodies of approaching workers.

  The design of the active space has evolved to communicate many kinds of information in addition to sex and recognition. Guard ants inform nestmates of the approach of enemies by releasing alarm substances. These chemicals are simple in structure compared to sex and trail pheromones. They are released in large quantities, and their active spaces travel far and fast. There is no need for privacy. On the contrary, there is good reason for friend and foe alike to smell them—and the sooner the better. The purpose is to stir alertness and action, and among as many nestmates as possible. Pumped-up fighters rush into the field upon detecting an alarm pheromone, while at the same time nurses carry the young deeper into the nest.

  A remarkable pheromone-and-allomone combination is used as a “propaganda substance” by an American species of slave-maker ant. Slavery is widespread in ants of the north temperate zone. It starts when colonies of the slave-making species conduct raids on other ant species. Their workers are shiftless at home, seldom engaging in any domestic chore. However, like indolent Spartan warriors of ancient Greece, they are also ferocious in combat. In some species the raiders are armed with powerful sickle-shaped mandibles capable of piercing the bodies of their opponents. During my research on ant slavery I found one species that uses a radically different method. The raiders carry a hugely enlarged gland reservoir in their abdomen (the rear segment of the three-part body) filled with an alarm substance. Upon breaching the victim’s nest, they spray large quantities of the pheromone through the chamber and galleries. The effect on the defenders of the allomone (or, more precisely, pseudo-pheromone) is confusion, panic, and retreat. They suffer the equivalent of our hearing a thunderously loud, persistent alarm coming from all directions. The invaders do not respond the same way. Instead, they are attracted to the pheromone, and as a result they are able easily to seize and carry away the young (in the pupal stage) of the defenders. When the captives emerge from the pupae as adults, they become imprinted, act as sisters of their captors, and serve them willingly as slaves for the rest of their lives.

  Ants are possibly the most advanced pheromonal creatures on Earth. They have more olfactory and other sensory receptors on their antennae than any other known kind of insect. They are also walking batteries of exocrine glands, each of which is specialized to produce different kinds of pheromones. In regulating their social lives they employ, according to species, from ten to twenty kinds of pheromones. Each one conveys a different meaning. And that is just the beginning of the information system. Pheromones can be discharged together to create more complex signals. When releas
ed at different times or in different places, their meaning changes yet another way. Still more information can be transmitted by varying the concentration of the molecules. In at least one American species of harvester ant I have studied, for example, a barely detectable level of pheromone evokes attention and movement by workers toward the source. A somewhat higher concentration causes the ants to search excitedly back and forth. The highest concentration of the substance, that occurring close to the signaling worker, causes a frenzied attack on any foreign organic object in the vicinity.

  Plants of some species communicate by pheromones. At least they are able to read the distress of neighboring plants by responding with actions of their own. A plant attacked by a serious enemy—bacteria, fungus, or insect—releases chemicals that suppress the invader. Some of the substances are volatile. They are “smelled” by their neighbors, who make the same defensive response even though they themselves are not yet under attack. Some species are assaulted by sap-sucking aphids, insects especially abundant in the north temperate zone and capable of wreaking heavy damage. The plant-generated airborne vapor not only stirs neighboring plants to secrete defensive chemicals, but also reaches small wasps that parasitize aphids, drawing them to the vicinity. A few species use yet another defensive line. The signals are transmitted from plant to plant along the strands of symbiotic fungi that entwine the roots and connect one plant to another.