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The Ghost of Protagoras

The Evolution of Culture in Animals

by John Tyler Bonner
Princeton University Press, 216 pp., $14.50

Man, the Promising Primate

by Peter J. Wilson
Yale University Press, 185 pp., $12.95

The female mason wasp, Monobia quadridens, excavates a broad chamber by digging a long tube into the pith of trees and stems. She deposits a series of eggs in the tube, starting at the bottom and separating each egg from the next by a curved mud partition. The partitions are shaped with their rough and convex side toward daylight and their smooth and concave side toward the cul de sac at the blind end of the chamber. The larvae feed and pupate within their chambers, which the mother has provisioned with food. When the young adults emerge, they crawl toward freedom by chewing through the rough, convex sides of the partitions. If the partitions are experimentally reversed, so that the rough and convex sides now point toward the cul de sac, the emerging adults cut their way into the stem, pile up at the blind end of the tube, and eventually die. Apparently, the mason wasp has evolved a rigidly programmed rule of behavior: cut through the rough and convex side of the partition. In nature, obedience to this rule always leads to daylight. If a human experimenter intervenes to reverse the partitions, the wasp cannot accommodate and digs to its own death, steadfastly obeying its unbreakable rule.

What the wasps lack (as Bonner tells this arresting story)—and what human beings possess in unparalleled abundance—is the common theme of both books: flexibility in behavioral response. Bonner defines culture as “the transfer of information by behavioral means,” and structures his fascinating book as a survey of culture in the animal kingdom, marching up the venerable chain of being toward bigger brains, increasing behavioral complexity, and freedom from rigid genetic programs specifying “single response behaviors.” Wilson identifies flexibility—that is, freedom from genetic programming of specific behaviors—as the key to our evolutionary promise; he traces the origins of human culture to the structural and nongenetic (but biologically based) rules that we follow in establishing systems of kinship.

Human flexibility has at least three complex and interrelated sources. First, we possess a brain much larger, in proper relation to the size of our bodies, than that of any other animal (except the bottle-nosed dolphin). More circuitry gives any computing machine a capacity for flexible response that increases (indeed explodes) at a far faster rate than the growth of its material substrate. A simple machine can handle tic-tac-toe; complex computers may soon be giving chess grand masters a run for it. The metaphor is somewhat mixed, but it is an arresting thought nonetheless that our brains contain more information, in an engineer’s technical sense, than all the DNA in our genes.

Second, we have evolved our massive brains largely by the evolutionary process of neoteny: the slowing down of developmental rates and the consequent retention to adulthood of traits that mark the juvenile stages of our ancestors. We retain the rapid fetal growth rate of neurons well beyond birth (when the brain of most mammals is nearly complete), and end up with the bulbous cranium and relatively large brain so characteristic of juvenile primates. Neoteny also slows down our maturation and gives us a long period of flexible childhood learning. I believe that the analogy between childhood wonder and adult creativity is good biology, not metaphor.

Third, as primates we belong to one of the few groups of mammals sufficiently unspecialized in bodily form to retain the morphological capacity for exploiting a broad range of environments and modes of life. A bat has committed its forelimbs to flight, a horse to running, and a whale to balancing and paddling. Culture and intelligence at a human level may have required the evolution of a free forelimb and a generalized hand endowed with the capacity to manufacture and manipulate tools (both from manus = hand). Only the morphologically unspecialized among mammals have not made inflexible commitments to particular modes of life that preclude this possible prerequisite for intelligence.

Despite their common emphasis on flexibility as the hallmark of humanity, Bonner and Wilson have written very different books from disparate intellectual traditions allied to their professional affiliations (Bonner is a Princeton biologist, and Wilson a New Zealand anthropologist). I must confess that, although I share Bonner’s profession, I find myself more attracted to Wilson’s position.

Ecologists and evolutionists complain bitterly that molecular biologists sometimes denigrate their subject by attempting to explain whole organisms in terms of the chemistry and physics of their constituent parts. Evolutionists decry this crass reductionism and defend the validity of their enterprise with appeals to pluralism and theories of hierarchical levels. Yet, like the boy who swore, when young, that he would never kick little kids off the basketball court when he grew up, but then couldn’t resist the power of maturity, evolutionists sometimes take as haughty an attitude toward the next level up the conventional array of disciplines: the human sciences. They decry the supposed atheoretical particularism of their anthropological colleagues and argue that all would be well if only the students of humanity regarded their subject as yet another animal and therefore yielded explanatory control to evolutionary biologists.

Bonner does sense his difficulty when mild odor of reductionism in a curious feature of its organization. Explicitly rejecting any discontinuity in nature as a violation of some preeminent principle of uniformity, Bonner admits to a personal necessity for discovering the true origins of human culture well before the evolutionary rise of man. He writes: “I am a uniformitarian and believe that all evolutionary changes were relatively gradual and that we can find the seeds of human culture in very early biological evolution.” He therefore begins with the motility of bacteria (quick and flexible behavioral reaction vs. slow genetic response) and, like Emerson’s worm, “mounts through all the spires of form” toward human flexibility. He arranges the facts of animal behavior according to their rank in a chain of being defined largely by increasing size of the brain. Bonner writes:

There is a direct inverse correlation with the time of appearance of a group in earth history and the size of its brain. At one end of the spectrum fish have small brains, while at the other end mammals have the largest. This suggests a trend toward increase in the ability to learn, toward an increase in the flexibility of the response.

Other criteria are also invoked, all loosely coordinated around the more-is-better principle. In one remarkable passage, Bonner ranks species of social insects by the size of their groups: “The reason for considering this a more advanced stage is that these colonies are larger, consisting of 300 to 80,000 individuals.” Perhaps the biggest giveaway occurs in what may be a slip, where Bonner abandons his usual, sufficiently dubious terminology of “higher” and “lower” organisms, and speaks of prehuman creatures as “lesser animals.”

If the chain of being were an ineluctable mode of organization, rather than (as I would maintain) an indefensible conceit, then Bonner’s continuationist perspective could scarcely be gainsaid. Life would move in a single direction and humans, on top, would be properly analyzed in biological terms as the improved inheritors of all that came before. But evolution is a copiously branching network, not a ladder, and I do not see how we, the titular spokesmen for a few thousand mammalian species, can claim superiority over three quarters of a million species of insects who will surely outlive us all, not to mention the bacteria, who have shown remarkable staying power for more than three billion years.

Bonner does sense his difficulty when he has to admit the undoubted success of his lesser creatures:

Even though mammals have been successful in this evolutionary trend, and primates the most successful of all, not all the other vertebrates, the fish, the amphibians, the reptiles, and the birds should become extinct. Selection, more especially in a complex environment, will find many successful solutions each of which correspond to the available ecological niches.

But perhaps the proper lesson of this observation simply affirms Darwin’s aphorism: “never say higher or lower.” And if we abandon the venerable chain of being, we lose the most promising frame for viewing human culture in biological terms as an extension, almost a necessary one, of longstanding evolutionary trends.

Bonner’s account also rests upon another reductionist tradition of argument—the atomistic and adaptationist style of modern Neo-Darwinism, which tends to dissolve entire organisms into constituent parts and to argue that most parts owe their form to direct shaping by natural selection. In this perspective, the problem of the evolution of culture lies in discovering the adaptive significance of each individual feature. Bonner largely accepts the extreme form of the argument popularized by Richard Dawkins in The Selfish Gene,1 and recently attacked with eloquence by Sewall Wright,2 a founder of population genetics, who, at age ninety, has been fighting this particular battle for more than half a century. Dawkins goes a step beyond reduction to parts and views genes themselves as the focus of natural selection. Bodies become mere “survival machines,” temporary homes for genes engaged in a more than metaphorical struggle to make more copies of themselves in future generations.

I find little defensible in this view. Selection cannot “see” genes, and can only work through the differential birth and death of individuals. Nearly all genes have multiple effects, many of them irrelevant to adaptation. Bodies are not an inventory of parts produced by individual genes, but integrated structures that cannot always be changed piecemeal by the dictates of selection. Organic forms are not an array of optimal adaptations to their immediate surroundings, but complex products of history, not always free to change in any direction that might “improve” them. When Bonner writes that “natural selection for optimal feeding is then presumed to be the cause of non-motility in all forms,” I can’t help suspecting that some plants might do even better if they could walk from shade to sun—but that inherited constraints of design never permitted a trial of this intriguing option.

This research tradition of adaptive explanation by parts, inherited from the declining Neo-Darwinian synthesis of evolutionary biology, defines the essence of sociobiology. In applying this style of argument to human beings, many sociobiologists fail to appreciate the interposition of nongenetic cultural transmission as a cause of behavior. They reify the human repertory of behaviors into “things” (aggression, xenophobia, homosexuality), posit selective advantages for each item (usually by telling a speculative story), and complete a circle of invalid inference by postulating genes, nurtured by natural selection, “for” each trait.

John Bonner is far too subtle a thinker to engage in such contentious nonsense. He wisely avoids, indeed opposes by his emphasis on human flexibility, any sociobiological explanation of specific human behaviors. But this very wisdom forces Bonner into a dilemma that prevents an otherwise charming book from becoming a masterpiece. For Bonner is committed to various forms of reductionism—to the continuationism of a gradually ascending chain of being linking humans to the rest of life, and to the sociobiological penchant for adaptive explanations based on a struggle among genes. But since he is wisely unwilling to extend the argument to details of human behavior, he is left with rather little to say about the biological basis of human culture—little, in fact, beyond the unexceptionable claim that we have inherited, through large brains, the capacity to develop complex culture, and that this capacity is highly adaptive. So what else is new?

Indeed, Bonner’s problem is the central dilemma of all human sociobiology. When it is injudicious and trades in speculative genetic arguments about specific human behaviors, it speaks nonsense. When it is judicious and implicates genetics only in setting the capacity for broad spectra of culturally conditioned behaviors, then it is not very enlightening. To me, such an irresolvable dilemma only indicates that this latest attempt to reduce the human sciences will have very limited utility.

At this point Bonner might reply, with some apparent justice, that I have been unfair to him. His book is about culture in “lower” animals, and doesn’t even have an explicit chapter on humans. And yet the ghost of Protagoras pervades the entire work, for man is the measure of all things. The decision to array animal cultures as a chain of being casts man as the inevitable referent for all. We stalk every page, often in silence. Read and enjoy this book as a deft and lucid account, filled with fascinating stories of natural history. But do not expect a revelation at the top.

Peter Wilson’s approach is entirely different. He also begins with a discussion of human biology, emphasizing the flexibility that arises from large brains, neoteny, and unspecialized morphology. But he then eschews any form of smooth extrapolation and argues that, while biology provides a necessary foundation, human culture represents a level of our lives that cannot be rendered in biological terms.

This antireductionist perspective is often attacked as obfuscating, if not downright mystical, by those of opposite persuasion. Bonner, albeit gently, caricatures the argument for an independence of human culture by writing:

It is a new condition that came into being as a result of the complexity of the mind of early man. To that extent the cultural anthropologist would consider it biological, but once it came into being, it took a life of its own, and its new properties cannot be understood in terms of the level below. It is, so to speak, self-propelled and, like a soul, has become detached from its body.

But the notion of hierarchical levels that cannot be reduced, one to the next below, is no appeal to mysticism. A claim for the independence of human culture is not an argument for its fundamental ineffability (like a soul), but only for the necessity of explaining it with principles different from the laws of evolutionary biology. New levels require an addition of principles; they neither deny nor contradict the explanations appropriate for lower levels. The principles of aesthetics do not preclude a chemical analysis of pigments in the Mona Lisa—but only a fool would invoke such chemistry to explain the essence of the lady’s appeal. In this sense, the notion of partially independent hierarchical levels of explanation strikes me as a statement of common sense, not mystery or philosophical mumbo-jumbo. I also regard it as an indispensable approach for the proper analysis of human culture.

We must, of course, be wary of the deepest cultural prejudice of all: our almost desperate desire to make human beings special and superior among the animals of our earth. We must therefore rigidly scrutinize any proposal for human uniqueness. We must recognize the elements of continuity that exist between the social behavior of human beings and other animals (as Bonner amply demonstrates); and we must note that some animals maintain rudimentary expressions of what we would call culture in humans. Still, when all this is said, we cannot stretch our ladder of extrapolation from amoebae to monkeys and up to people. We are not better, but we are different because change in the basic fabric of our social systems occurs, as it does in no other animal, by the nongenetic transmission of information across generations—in short, by culture. (Yes, some birds teach song to their offspring, and songs may alter by cultural tradition over generations—but major change in the basic structure of animal societies requires genetic modification.)

Darwinian—and all biological—theories of evolutionary change are, fundamentally, propositions about modes of genetic modification. What else could they be? Human cultural evolution proceeds along paths outstandingly different from the ways of genetic change. Biologists believe that genetic change is primarily Darwinian—that is, it occurs via natural selection operating upon undirected variation. Human cultural evolution is Lamarckian—the useful discoveries of one generation are passed directly to offspring by writing, teaching, and so forth. Biological evolution is constantly diverging; once lineages become separate, they cannot amalgamate (except in the production of new species by hybridization—a process that virtually never occurs in animals). Trees are correct representations of biological evolution.

In human cultural evolution, on the other hand, transmission and anastomosis are rampant. Five minutes with a wheel, a snowshoe, a bobbin, or a bow and arrow may allow an artisan of one culture to capture a major achievement of another. Fruitful analogies may be drawn between biological and cultural evolution, but they remain analogies. The processes are different, even though human culture has a biological base. Cultural evolution needs laws of its own. This is neither a council of despair nor a dashing of hopes for intellectual coherence. It is merely an acknowledgment of the world’s hierarchical structure and, I hope, an intellectual challenge in its own right.

As an outsider to his profession, I cannot judge Wilson’s particular argument for tracing a major root of human culture to the origins of kinship. But I do note that his style of explanation conforms to the hierarchical model that I find indispensable for analyzing human culture. Wilson does not eschew biology. In fact, he begins with biology and invokes it as a foundation in two senses, general and specific. We are “the promising primate” because our biological flexibility permits us to enter (for the first time in life’s history on earth) the rapid and accelerating world of Lamarckian cultural evolution. More specifically, we develop kinship (from which our basic social structure arises by extension) by producing an intersection between two fundamental, biological relationships. The “primary bond” links mother and child; the “pair bond” unites adult male and female. Other primates base their social groupings on one or the other, but do not combine them in any tightly integrated way.

The pivotal, and only common, figure in both bonds is the adult female. The missing concept, while the bonds remain separate, is fatherhood. Mammalian mothers must nurture their children, and (obviously) males and females must unite to produce offspring. But fatherhood, defined as nurturance by males rather than mere stud service, does not represent a biological necessity. Wilson argues that the concept of fatherhood arose in creatures sufficiently brainy to abstract the general principle of “relationship” and therefore to conjoin primary and pair bonds. Once the abstract principle of intersecting two relationships to form a third is grasped, it may be extended further to produce complex social groupings based on kinship. Wilson locates the foundations of human social organization in this structural nonbiological rule and writes:

If it is possible to create a relationship by combining two others, then the principle of transitivity emerges, by which a link between two individuals may be transferred to a third…. If it is possible to create the relationship of father by conjoining the pair and primary bonds, then since sex and generation boundaries have been crossed, there are no barriers left. The relations between any two individuals can be continued indefinitely by linking through the common member(s). The extension of the primary bond and the lengthening of the pair bond lead to a junction that is the elementary basis for a generalized social organization typical of the human species. For it is only then that kinship is possible, and with kinship we have the most flexible, generalized, and adaptable principle of group organization in the primate order.

The argument is based on biology—both the existence of pair and primary bonds and the braininess to grasp their abstract connection. But the result—the notion of fatherhood and the extension of its principle to systems of kinship—is not, in itself, a Darwinian phenomenon (though it has consequences for survival—and culture feeds back upon biology). As Wilson writes: “It is a distinguishing feature of the human species that although individuals are naturally impelled toward living in company and it is necessary for them to do so, there is no universal instinctive form that this company will take.”

Wilson’s title is a conscious double entendre. Human beings are promising because their flexibility opens so many options. But the promise also assumes a more specific function. A woman cannot always play both roles of partner and mother simultaneously. She must often hold one in temporary abeyance. To secure the momentarily neglected role, she must make a form of representation indicating her future attention to it—in short a promise. Recognition of a promise requires the brain power to make abstractions and to develop a notion of the future. Wilson views the structural necessity for promising as a possible impetus to consciousness.

I am not taken by all of Wilson’s methodology. He works in the tradition of Hobbes or Rousseau, arguing by presupposition and logic, rather than by empirical contact with the world. I am enough of a hide-bound Anglo-Saxon pragmatist to wonder about the ultimate worth of this older, speculative tradition. Still, I regard Wilson’s work as promising in a third sense, for it acknowledges the legitimate uniqueness of human culture and extends a welcoming hand to biology at the same time. It debars the imperialistic designs of some biologists upon the human sciences, while it affirms as necessary the insights from Darwin’s world. True partnership without engulfment or ignorance; I see no other path to a satisfactory science of man.

  1. 1

    Oxford University Press, 1976.

  2. 2

    Sewall Wright, “Genic and organismal selection,” Evolution, Vol. 34, 1980, pp. 825-843.

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